Cullen and Evans BMC Ecol (2016) 16:52 DOI 10.1186/s12898-016-0106-8 BMC Ecology

RESEARCH ARTICLE Open Access Palaeoenvironmental drivers of vertebrate community composition in the Belly River Group (Campanian) of Alberta, Canada, with implications for dinosaur biogeography Thomas M. Cullen1,2* and David C. Evans1,2

Abstract Background: The Belly River Group of southern Alberta is one of the best-sampled Late Cretaceous terrestrial faunal assemblages in the world. This system provides a high-resolution biostratigraphic record of terrestrial verte- brate diversity and faunal turnover, and it has considerable potential to be a model system for testing hypotheses of dinosaur palaeoecological dynamics, including important aspects of palaeoecommunity structure, trophic interac- tions, and responses to environmental change. Vertebrate fossil microsites (assemblages of small bones and teeth concentrated together over a relatively short time and thought to be representative of community composition) offer an unparalleled dataset to better test these hypotheses by ameliorating problems of sample size, geography, and chronostratigraphic control that hamper other palaeoecological analyses. Here, we assembled a comprehensive rela- tive abundance dataset of microsites sampled from the entire Belly River Group and performed a series of analyses to test the influence of environmental factors on site and taxon clustering, and assess the stability of faunal community composition both temporally and spatially. We also test the idea that populations of large dinosaur taxa were particu- larly sensitive to small-scale environmental gradients, such as the paralic (coastal) to alluvial (inland) regimes present within the time-equivalent depositional basin of the upper Oldman and lower Dinosaur Park Formations. Results: Palaeoenvironment (i.e. reconstructed environmental conditions, related to relative amount of alluvial, fluvial, and coastal influence in associated sedimentary strata) was found to be strongly associated with clustering of sites by relative-abundance faunal assemblages, particularly in relation to changes in faunal assemblage composition and marine-terrestrial environmental transitions. Palaeogeography/palaeolandscape were moderately associated to site relative abundance assemblage clustering, with depositional setting and time (i.e. vertical position within strati- graphic unit) more weakly associated. Interestingly, while vertebrate relative abundance assemblages as a whole were strongly correlated with these marine-terrestrial transitions, the dinosaur communities do not appear to be particu- larly sensitive to them. Conclusions: This analysis confirms that depositional setting (i.e. the sediment type/sorting and associated char- acteristics) has little effect on faunal assemblage composition, in contrast to the effect of changes in the broader palaeoenvironment (e.g. upper vs. lower coastal plain, etc.), with marine-terrestrial transitions driving temporal faunal dynamics within the Belly River Group. The similarity of the dinosaur faunal assemblages between the time-equivalent

*Correspondence: [email protected] 1 Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada Full list of author information is available at the end of the article

© The Author(s) 2016. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Cullen and Evans BMC Ecol (2016) 16:52 Page 2 of 35

portions of the Dinosaur Park Formation and Oldman Formation suggests that either these palaeoenvironments are more similar than characterized in the literature, or that the dinosaurs are less sensitive to variation in palaeoenviron- ment than has often been suggested. A lack of sensitivity to subtle environmental gradients casts doubt on these forces acting as a driver of altitudinal zonation of dinosaur communities in the Late Cretaceous of North America. Keywords: Palaeoenvironments, Vertebrate microfossil sites, Palaeoecology, Altitudinal sensitivity, Biogeography, Dinosaurs, Faunal turnover, Latitudinal climate gradients, Belly River Group

Background by very low sample sizes [24, 43, 47], though ongoing Differences in faunal composition in the Late Cretaceous work collecting new specimens, relocating these sites, of Western North America have been hypothesized to and incorporating them into the broader stratigraphy is reflect adaptation to latitudinal and altitudinal climatic ameliorating some of these issues [23, 24, 43, 44, 48]. gradients [1–7]. Environmental changes caused by trans- The Belly River Group of southern Alberta is one of the gression-regression cycles of the Western Interior Sea best-sampled Late Cretaceous vertebrate fossil deposits have been suggested to drive the high diversity and high in the world [44], providing a high-resolution biostrati- faunal turnover rates of non-avian dinosaurs [4, 5, 8–11], graphic record of terrestrial vertebrate diversity and along with changes in the vertebrate community struc- faunal turnover, and has considerable potential to be as ture more generally [12–16]. However, global-scale anal- a model system for testing hypotheses of dinosaur pal- yses of dinosaurs, as a whole [17] and at the family level aeoecological dynamics, including important aspects of [18], indicate that large-scale changes in sea level may palaeoecommunity structure, trophic interactions, and not have had a significant influence on broad patterns of responses to environmental change [48]. The Belly River diversity, evolution, or migration. This suggests that puta- Group is composed of the Foremost, Oldman, and Dino- tive patterns in dinosaur ecology and evolution related to saur Park formations, and spans a large portion of the sea level, such as those described from Western North Campanian from a period of time from approximately America, may be either the result of other factors, such 79–74 Ma [1, 49, 50]. The full extent of the Belly River as sampling biases, or may be occurring on a scale that Group records two major regional sea level changes is too small to be readily detected in such coarse-scale in the Western Interior Seaway (the relatively shal- analyses [4]. Previous studies have suggested that the low, inland seaway that at its greatest extent stretched composition and diversity of taxa recovered from spe- from the Arctic Ocean to the Gulf of Mexico), the first cific fossil localities across Western North America var- of which is a regressive event in the Foremost and lower ies depending on their distance from the palaeoshoreline Oldman formations, and the second of which is a major of the Western Interior Sea [1–3, 5, 7, 19, 20]. This has transgressive event recorded in the uppermost Oldman led to considerable debate regarding the degree of pro- and Dinosaur Park formations that marks the transi- vinciality/endemism in dinosaur populations [1–7, 9, 10, tion between the Belly River Group and the overlying 14, 15, 19–28], the putatively high diversity and restricted Bearpaw Formation [49, 50]. The Foremost Formation range of dinosaur taxa when compared to modern large is the stratigraphically lowest unit within the Belly River mammals [2, 5, 7, 19, 20, 22, 29–37], as well as discus- Group, and conformably overlies the marine shales of sions of niche-partitioning in dinosaurs across environ- the Pakowki Formation. The earliest Foremost sediments mental gradients in a single depositional basin [2, 5, 10, show considerable marine influence, and the formation, 19, 20, 23, 24, 29, 30, 38–45]. These noted variations in going from lowest to highest outcrops, is generally com- palaeocommunities over sub-million year timeframes posed of paralic to non-marine sediments, following a and over relatively small palaeogeographic areas suggests coarsening upwards succession [50, 51]. Conformably that many taxa, but particularly large-bodied dinosaurs, overlying the Foremost Formation is the Oldman For- may have been sensitive to palaeoclimatic and palaeoen- mation. The Oldman Formation is broadly considered vironmental change [1–3, 5, 7, 9, 43, 44, 46]. However, to represent more fluvial, inland conditions, and is made this model has been challenged for reliance on data up of series of upward fining palaeochannel sandstone derived from disjunct geographic areas that are poorly successions, with a variety of channel top, channel mar- constrained chronostratigraphically [28]. the ability to gin, and overbank facies [12, 14, 50, 52]. The amount of test hypotheses about dinosaur biogeography, endemism, exposure of upper Oldman sediments is dependent on and environmental sensitivity has historically been diffi- sampling location, with southern sites showing a thick cult, as many specimens were collected with only limited succession of strata, and northern sites truncated above geological data or stratigraphic information, and known the middle Oldman by a regional disconformity [14, Cullen and Evans BMC Ecol (2016) 16:52 Page 3 of 35

50]. To the north, upper Oldman Formation strata are [14, 16, 52, 59, 60]. While vertebrate microfossil sites in a replaced disconformably by those of the Dinosaur Park given area or formation may represent the same broader Formation as a result of clastic-wedge replacement [50]. palaeoenvironment (e.g. upland fluvial system, lowland The Dinosaur Park Formation (DPF) is considered to coastal plain, etc.), their method of deposition may dif- have a greater coastal influence than the underlying Old- fer (e.g. flow rates, depositional energy, sediment size/ man Formation (OM), and is characterized by sandy to sorting, etc.), and this has led to concerns that microsites muddy, alluvial, estuarine, and paralic facies [12, 49, 50, with differing depositional setting may not preserve com- 52]. The transition to more marine environment in the parable vertebrate material or faunal assemblages [14, upper Dinosaur Park Formation is marked by the deposi- 59]. These concerns regarding the effect of depositional tion of the Lethbridge Coal Zone (LCZ), which interfin- setting on the presence/absence and ranked abundances gers with and is overlain by marine shales of the Bearpaw of taxa at a given microvertebrate site have been partially Formation [13, 49, 53]. The pre-LCZ section of the Dino- lessened by a new taphonomic model for microsite for- saur Park Formation in Dinosaur Provincial Park (DPP) is mation suggesting that depositional setting may not play thought to be broadly time-equivalent to the upper Old- a large role when comparing sites of different type, as man Formation in the Milk River/Manyberries (MRM) channel deposits may represent the short-term erosion regions of southern Alberta [14, 50]. The muddy strata of and local re-deposition of lower-energy pond depos- the upper Oldman Formation in Milk River/Manyberries its [59]. Microsite studies in the Belly River Group of are typically thought to be more environmentally similar Alberta have so far focused on identifying the taxa pre- to that of the middle Oldman ‘Comrey sandstone’ (repre- sent across the region, and assessing any broad trends or senting a more seasonally arid, inland, fully non-marine associations that may be present through specific strati- fluvial landscape) than to the time-equivalent pre-LCZ graphic intervals [8, 12–14, 16, 53, 58, 61]. These studies Dinosaur Park Formation in DPP (representing a wetter, have identified aquatic and terrestrial communities, along more marine-influenced coastal plain) [14, 49, 50]. This with some evidence of potential endemism. Additionally, view has been questioned by other studies suggesting they have demonstrated that terrestrial-marine environ- the time-equivalent Oldman and Dinosaur Park forma- mental transitions drive at least some of the changes in tions share a generally wet, coastal environment and that vertebrate faunal assemblages, such as an increase in variations in recorded wet-dry signal may represent sea- ceratopsid dinosaur abundance correlated with increas- sonality and/or spatial variation in local habitat [22, 54]. ing marine influence in the Dinosaur Park Formation of Interpreting these units is complicated by the existence DPP [8], and an inverse relationship between sharks and of heterogeneity in their geographic extent and palaeoen- lissamphibian abundances in the Foremost Formation vironment through time, particularly in their relation to [16]. However, major quantitative studies have focused the shore of the Western Interior Seaway [5, 8, 19, 20, 24]. on either the transgressive or regressive sequences, and Meaningful comparison between these units requires not the entirety of the Belly River Group, resulting in detailed chronostratigraphic control to mitigate the our understanding of the environmental drivers behind confounding effects of temporal changes in community microsite faunal assemblage structure remaining incom- structure. This is particularly important because the dis- plete despite the abundance and quality of the available tribution of dinosaurs has been hypothesized to be sen- data. In addition, new data suggests that dinosaur spe- sitive to even small-scale palaeoenvironment differences, cies found in the Dinosaur Park Formation of DPP are such as those between the lower and upper coastal plain also found in the time-equivalent sections of the Old- settings of the time-equivalent Oldman and Dinosaur man Formation in MRM [22, 24]. These units have been Park formations [5, 14, 24, 50, 52]. described as representing different palaeoenvironmental Vertebrate microfossil sites from the Belly River Group regimes [14, 22, 24, 50]. However, the Oldman Formation have provided a wealth of knowledge on vertebrate pal- is palaeoenvironmentally dynamic throughout its his- aeoecology [12, 14, 15, 52, 55, 56]. Vertebrate microfos- tory, shifting from lowland coastal plain to more inland sil sites, sensu [57], are useful in overcoming issues of braided rivers, and back to lowland coastal plain [14, 16, low sample size that commonly hinder palaeontological 22, 50]. As a result, comparisons of vertebrate microfossil investigations, as they are both abundant and each site sites can provide an important test of habitat sensitivity can preserve large numbers of small teeth, bones, and in dinosaurs. scales of numerous taxa thought to represent much of the Given the ongoing debate regarding the putatively vertebrate community composition of a given area [12– narrow associations of dinosaurs with particular envi- 16, 53, 55, 58]. These sites are concentrated in a number ronments, locations, and/or geological formations, this of ways, with most representing in-channel deposits, cre- study uses the largest Cretaceous vertebrate micro- vasse splays, low energy ponds, or shoreface lag deposits site dataset yet assembled to first test the previously Cullen and Evans BMC Ecol (2016) 16:52 Page 4 of 35

suggested associations between faunal assemblages to their theoretical optimum. Rarefied data were fur- and differing environments, and then use those as a ther Wisconsin double standardized after conversion proxy to test for differences in dinosaur assemblages in to relative abundances, again through use of the func- the time-equivalent sections of the Dinosaur Park and tions contained in the ‘vegan’ package [65]. The stand- Oldman formations. We hypothesize that altitudinal ardized relative abundance dataset was converted to the (inland vs. coastal) effects will act as the largest driver percentage-difference dissimilarity index (also referred of faunal assemblage change, following previous results to as Bray-Curtis) [66]. R- vs. Q-mode cluster analyses on more limited datasets, with other taphonomic or were generated for the resultant dissimilarity dataset, temporal effects acting minimally on the preserved with UPGMA linkage, using the ‘tabasco’ function of the ecological signal. We also hypothesize that dinosaurs, ‘vegan’ R package [65]. DPP and Milk River sites were particularly those of large body size, will not be sensi- identified on the resulting plots, and major site/taxon tive to altitudinal change as recorded in the Belly River clusters were highlighted. Group. Although it is frequently hypothesized that The R- vs. Q-mode cluster analysis was repeated for large dinosaurs are sensitive to environmental variation three sub-sample analyses focused on the time-equiva- [1–9, 11, 14, 15, 19–24, 26, 27, 42, 43, 62], many groups lent upper Oldman and Dinosaur Park formations, one of large mammals today are resilient to environmental including only dinosaur proportions, another including variation and have broad latitudinal distributions [2, 7, only theropod proportions, and a third including pro- 32]. portions of all non-dinosaurs shared between these sites. The first two subsamples contained different source data Methods (Additional file 1) for Dinosaur Provincial Park sites than Dataset integration and taxonomic consistency the comparisons of total vertebrate assemblages, being A dataset (Table 1) of vertebrate microfossil taxon abun- derived from the re-sampled dinosaur material of Brink- dance for Belly River Group sites (N = 48) was created man et al. [8] instead of Brinkman [12]. The dataset of through the merger of multiple literature sources [12– Brinkman et al. [8] allows for more detailed taxonomic 14, 16, 53, 58, 61]. These sites span the duration of the comparisons when restricted to dinosaur data (due to the Belly River Group (BRG), and were sampled spatially inclusion of several additional small theropod genera), from Dinosaur Provincial Park (DPP) and from the area but is not considered appropriate for the broader verte- around the Milk River south of Manyberries (MRM) brate faunal comparisons due to the lack of methodologi- (Fig. 1). Some revision to the taxonomic categories was cal consistency (associated with the targeted nature of required in order to successfully merge these datasets, this additional dinosaur sampling) relative to the faunal with specific changes related to differences in the inclu- data for other vertebrate material in Dinosaur Provincial sivity of taxonomic categories in each source dataset (e.g. Park sites. The non-dinosaur subsample used the same ‘mammals’ vs. genus-level assignment of respective taxa, source data as the primary analysis of all vertebrates, due to a lack of genus resolution in included DPP data; the only difference being the removal of dinosaurs from inclusion of specimens of Allocaudata within Caudata in the dataset. This last analysis was performed to confirm early studies and separation in later studies, Brinkman the effect of dinosaurs on overall trends in the data, and pers. comm. 2016), updating terminology to reflect more avoid possible issues of circularity in interpreting the recent taxonomic revisions (e.g. Atractosteus to Lepisos- dinosaur data in isolation. teus for BRG gars, ‘teleost D’ to Coriops), noting areas of potential future taxonomic revision (e.g. Myledaphus to Environmental factors and redundancy analysis Myledaphus + Pseudomyledaphus, as the latter may exist Data relating to the palaeoenvironmental setting (marine, in multiple sites under the former name), and revisions to transitional, terrestrial—paralic/lower coastal plain, ter- identifications based on discussions with the collectors of restrial—alluvial/upper coastal plain), palaeogeography the source microsite data (e.g. Pachycephalosaur material (Dinosaur Provincial Park localities, Milk River locali- being now referred to hypsilophodont, Brinkman pers. ties), stratigraphic interval (Foremost Formation, lower comm. 2016) [14, 16, 63, 64]. Oldman Formation, middle Oldman Formation or ‘Com- rey sandstone’, time-equivalent upper Oldman and pre- Dataset standardization and R‑ vs. Q‑mode cluster analysis LCZ Dinosaur Park formations, Lethbridge Coal Zone The combined data matrix was rarefied in R using func- of Dinosaur Park Formation), and depositional setting tions contained within the ‘vegan’ package [65]. This was (shoreface deposit, crevasse splay deposit, in-channel done to compare sampling intensity between sites, and deposit) were taken from the literature [12–14, 16, 52, found that few sample issues exist between sites, though 53, 58, 61] and assembled into an environmental data most sites are likely somewhat undersampled compared matrix (Additional file 2). Though the palaeogeographical Cullen and Evans BMC Ecol (2016) 16:52 Page 5 of 35 ‑ Elasmo branchii indet. 2 4 0 0 0 0 0 0 0 0 0 0 0 0 0 Squatina 27 Chiloscyl - lium 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Ischyrhiza 12 16 Rhinoba - tos 0 3 0 0 0 0 0 0 - Synecho dus 0 0 0 0 0 0 0 0 ‑ 3 0 0 0 0 0 0 Orectolo bidae 38 - 0 0 0 0 0 0 Archae olamna 46 37 0 0 0 0 0 0 0 - Cretol amna 12 5 0 0 0 0 0 0 ‑ Odontas pididae 91 - Centro phoroides 0 0 0 0 0 0 0 0 2 0 0 2 0 0 Hybodus 49 88 0 0 0 0 0 0 79 - Protoplat yrhina 356 - 55 496 243 129 354 948 107 Myleda - + Pseudo phus myledaphus 1019 Taxon abundance table for each site analyzed in this study, with information derived and standardized from literature [ 12 – 14 , 16 53 58 61 ] from literature and standardized derived with information in this study, analyzed site table for each abundance Taxon (DPF/ LCZ; DPP) (DPF/ LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) BB96 L2377 BB115 BB119 BB108 BB102 BB94 BB75 1 Table Taxon Site Cullen and Evans BMC Ecol (2016) 16:52 Page 6 of 35 ‑ Elasmo branchii indet. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Squatina Chiloscyl - lium 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Ischyrhiza Rhinoba - tos 0 0 0 0 0 0 0 0 0 - Synecho dus 0 0 0 0 0 0 0 0 0 ‑ 0 0 0 0 0 0 0 0 0 Orectolo bidae - 0 0 0 0 0 0 0 0 0 Archae olamna 0 0 0 0 0 0 0 0 0 - Cretol amna 0 0 0 0 0 0 0 0 0 ‑ Odontas pididae - Centro phoroides 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Hybodus 0 0 0 0 0 0 0 0 0 - Protoplat yrhina - 6 13 54 61 92 218 228 110 657 Myleda - + Pseudo phus myledaphus continued (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) BB54 BB120 BB106 BB25 BB117 BB78 BB104 BB97 BB86 1 Table Taxon Cullen and Evans BMC Ecol (2016) 16:52 Page 7 of 35 ‑ Elasmo branchii indet. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Squatina Chiloscyl - lium 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Ischyrhiza Rhinoba - tos 0 0 0 0 0 0 0 0 0 - Synecho dus 0 0 0 0 0 0 0 0 0 ‑ 0 0 0 0 0 0 0 0 0 Orectolo bidae - 0 0 0 0 0 0 0 0 0 Archae olamna 0 0 0 0 0 0 0 0 0 - Cretol amna 0 0 0 0 0 0 0 0 0 ‑ Odontas pididae - Centro phoroides 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Hybodus 0 0 0 0 0 0 0 0 0 - Protoplat yrhina - 9 9 2 54 34 68 93 52 163 Myleda - + Pseudo phus myledaphus continued ------(DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (DPF/ pre- LCZ; DPP) (OM/ Com rey; DPP) (OM/ Com rey; DPP) (OM/ Com rey; DPP) (OM/ Com rey; DPP) (OM/ Com rey; DPP) (OM/ Com rey; DPP) BB51 BB31 BB98 BB107 BB100 BB103 BB121 BB71 BB118 1 Table Taxon Cullen and Evans BMC Ecol (2016) 16:52 Page 8 of 35 ‑ Elasmo branchii indet. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Squatina Chiloscyl - lium 0 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Ischyrhiza Rhinoba - tos 0 0 0 0 0 0 0 0 0 0 0 0 - Synecho dus 0 0 0 0 0 0 0 0 0 0 0 0 ‑ 0 0 0 0 0 0 0 0 0 0 0 0 Orectolo bidae - 0 0 0 0 0 0 0 0 0 0 0 0 Archae olamna 0 0 0 0 0 0 0 0 0 0 0 0 - Cretol amna 0 0 0 0 0 0 0 0 0 0 0 0 ‑ Odontas pididae - Centro phoroides 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Hybodus 0 0 0 0 0 0 0 0 0 0 0 0 - Protoplat yrhina - 2 0 1 2 6 2 0 1 2 20 14 102 Myleda - + Pseudo phus myledaphus continued - - (OM/ Com rey; DPP) upper; MRM) upper; MRM) (OM/ upper; MRM) upper; MRM) upper; MRM) upper; MRM) upper; MRM) (OM/ upper; MRM) (OM/ upper; MRM) upper; MRM) Com rey; MRM) BB105 PLS (OM/ HAS (OM/ BMC SalS (OM/ CS (OM/ HS (OM/ RDS (OM/ CN-1 CN-2 CBC (OM/ ORS (OM/ 1 Table Taxon Cullen and Evans BMC Ecol (2016) 16:52 Page 9 of 35 ‑ 0 0 Anura Elasmo branchii indet. 0 0 0 0 0 0 2 0 0 690 3 0 Teleostei 0 0 0 0 0 0 0 1 8 Squatina 34 0 0 Coriops Chiloscyl - lium 0 0 1 1 0 5 0 0 6 0 0 4 Enchodus 0 0 0 0 0 0 0 8 Ischyrhiza 16 20 0 0 Esocidae Rhinoba - tos 0 0 0 0 0 0 0 0 9 3 0 0 Paratarpon - Synecho dus 0 0 0 0 0 0 0 0 1 10 ‑ 679 215 ‑ Phyllodonti dae 0 0 0 0 0 0 0 0 1 5 Orectolo bidae 0 0 Amiidae - 0 0 0 0 0 0 3 0 Archae olamna 10 27 0 0 Lepisosteus - 0 0 0 0 0 0 0 0 0 4 - Cretol amna 0 0 Belonosto mus 0 0 0 0 0 0 2 ‑ Odontas pididae 23 79 50 - 1 ‑ Acipenseri formes 14 Centro phoroides 0 0 0 0 0 0 0 0 0 15 0 0 0 0 0 0 0 0 1 ‘Holostean ‘Holostean B’ Hybodus 10 15 18 0 0 0 0 0 0 0 0 0 0 0 - Protoplat yrhina 382 ‘Holostean ‘Holostean A’ - 8 9 5 19 24 15 29 40 Elasmodus sp. 235 Myleda - + Pseudo phus myledaphus 1952 2164 3780 - continued - - - - LCZ; DPP) LCZ; LCZ; DPP) LCZ; lower; MRM) lower; MRM) (OM/ lower; MRM) lower; MRM) lower; MRM) most; MRM) most; MRM) (Fore most; MRM) (Fore most; MRM) (Fore most; MRM) L2377 (DPF/ BB96 (DPF/ PHS (OM/ EZ (OM/ PHR93-2 WS (OM/ HoS (OM/ SPS (Fore PK (Fore PHR-1 PHR-2 PHRN 1 Table Taxon Taxon Site Cullen and Evans BMC Ecol (2016) 16:52 Page 10 of 35 8 8 2 3 7 1 0 35 112 24 13 29 14 23 Anura 4 1 3 40 57 19 28 49 32 11 15 56 163 331 Teleostei 3 6 8 4 2 1 0 1 16 33 56 47 17 155 Coriops 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Enchodus 8 3 4 4 3 6 3 2 5 1 0 14 35 14 Esocidae 0 0 0 0 0 0 0 0 1 0 0 0 0 1 Paratarpon 6 4 1 6 4 4 6 6 22 35 12 13 36 16 ‑ Phyllodonti dae 7 5 3 7 9 2 5 1 1 0 42 12 18 149 Amiidae 62 16 41 29 91 90 39 130 155 742 157 161 204 2714 Lepisosteus - 3 3 0 6 6 1 5 5 2 2 16 10 22 13 Belonosto mus 0 7 0 1 1 4 8 5 0 1 2 15 39 10 ‑ Acipenseri formes 1 3 0 0 1 0 1 1 1 0 2 3 11 196 ‘Holostean ‘Holostean B’ 0 86 17 80 66 44 13 26 213 175 105 116 668 1582 ‘Holostean ‘Holostean A’ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Elasmodus sp. continued pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) BB97 (DPF/ BB104 (DPF/ BB78 (DPF/ BB117 (DPF/ BB25 (DPF/ BB106 (DPF/ BB120 (DPF/ BB54 (DPF/ BB75 (DPF/ BB102 (DPF/ BB94 (DPF/ BB108 (DPF/ BB119 (DPF/ BB115 (DPF/ Taxon 1 Table Cullen and Evans BMC Ecol (2016) 16:52 Page 11 of 35 5 6 35 15 92 20 89 77 85 24 65 20 64 177 Anura 1 10 26 51 15 60 63 79 141 109 213 136 119 190 Teleostei 2 0 7 6 41 20 34 73 25 30 33 23 65 123 Coriops 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Enchodus 0 5 5 0 2 6 2 10 16 15 17 10 12 16 Esocidae 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Paratarpon 0 8 2 9 2 3 6 3 4 11 14 14 10 11 ‑ Phyllodonti dae 0 3 3 6 9 17 11 17 16 18 11 28 19 58 Amiidae 6 4 3 30 46 12 46 48 19 10 25 126 152 379 Lepisosteus - 0 0 0 0 0 1 0 2 8 1 0 8 10 Belonosto mus 12 0 0 0 0 0 3 0 9 5 3 1 0 6 9 ‑ Acipenseri formes 0 0 0 0 0 0 0 0 0 0 0 0 0 6 ‘Holostean ‘Holostean B’ 0 9 32 36 62 212 105 359 268 334 255 124 218 223 ‘Holostean ‘Holostean A’ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Elasmodus sp. continued upper; MRM) upper; MRM) Comrey; DPP) upper; MRM) Comrey; DPP) Comrey; DPP) Comrey; DPP) Comrey; DPP) Comrey; DPP) Comrey; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) HAS (OM/ BMC (OM/ BB105 (OM/ PLS (OM/ BB118 (OM/ BB71 (OM/ BB103 (OM/ BB121 (OM/ BB100 (OM/ BB107 (OM/ BB31 (DPF/ BB98 (DPF/ BB51 (DPF/ BB86 (DPF/ 1 Table Taxon Cullen and Evans BMC Ecol (2016) 16:52 Page 12 of 35 47 24 75 70 43 29 33 33 147 102 90 44 66 40 Anura 6 46 36 73 34 48 100 225 101 150 148 144 230 197 Teleostei 8 22 67 63 43 42 35 32 13 16 48 22 20 18 Coriops 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Enchodus 7 6 4 1 2 7 29 15 10 10 15 22 13 18 Esocidae 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Paratarpon 8 2 0 9 9 4 0 12 16 19 45 12 16 139 ‑ Phyllodonti dae 5 0 7 0 0 1 0 2 0 10 11 14 18 44 Amiidae 0 10 14 30 10 204 404 126 147 339 123 107 169 1001 Lepisosteus - 0 0 0 0 0 6 0 0 0 0 0 0 0 11 Belonosto mus 6 0 4 0 6 0 0 0 0 0 0 0 0 14 ‑ Acipenseri formes 0 5 4 0 0 0 0 0 0 0 0 0 45 25 ‘Holostean ‘Holostean B’ 1 1 5 54 31 19 55 73 57 36 49 32 229 138 ‘Holostean ‘Holostean A’ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Elasmodus sp. - continued most; MRM) lower; MRM) lower; MRM) (OM/ lower; MRM) lower; MRM) lower; MRM) upper; MRM) Comrey; MRM) upper; MRM) upper; MRM) upper; MRM) upper; MRM) upper; MRM) upper; MRM) SPS (Fore HoS (OM/ WS (OM/ PHR93-2 EZ (OM/ PHS (OM/ CBC (OM/ ORS (OM/ CN-2 (OM/ RDS (OM/ CN-1 (OM/ HS (OM/ CS (OM/ SalS (OM/ Taxon 1 Table Cullen and Evans BMC Ecol (2016) 16:52 Page 13 of 35 1 10 31 33 Anura ‑ Ceratopsi dae 1 0 0 8 6 37 1 89 305 265 Teleostei Eusuchia 1 1 15 29 96 414 0 0 30 10 Coriops - Champso saurus 0 1 14 15 7 93 0 0 0 0 Enchodus 0 7 4 0 Baenidae 0 0 3 1 4 47 Esocidae ‑ Chelydri dae 0 0 0 1 3 13 0 0 0 0 Paratarpon Adocus 0 0 0 0 0 0 0 2281 2016 1156 ‑ Phyllodonti dae ‑ Trionychi dae 0 0 8 15 10 79 0 9 0 17 Amiidae Basilemys 0 0 1 0 2 2 43 143 834 2463 Lepisosteus - Solemydidae 0 0 0 0 0 0 0 0 160 185 Belonosto mus ‑ Tes tudines indet. 0 0 0 0 0 0 2 0 25 90 ‑ Acipenseri formes ‑ Plesiosau ria 2 1 0 0 0 0 6 56 166 355 ‘Holostean ‘Holostean B’ Squamata 0 0 3 0 11 69 8 0 22 94 ‘Holostean ‘Holostean A’ Mosasauri ‑ dae 1 0 0 0 0 0 0 0 0 4 Elasmodus sp. Caudata + Caudata ‑ Allocau data 0 0 13 13 25 244 - continued - - - most; MRM) (Fore most; MRM) (Fore most; MRM) most; MRM) LCZ; LCZ; DPP) (DPF/ LCZ; DPP) (DPF/ pre-LCZ; DPP) (DPF/ pre-LCZ; DPP) (DPF/ pre-LCZ; DPP) (DPF/ pre-LCZ; DPP) PHRN (Fore PHR-2 PHR-1 PK (Fore BB96 (DPF/ L2377 BB115 BB119 BB108 BB102 1 Table Taxon Taxon Site Cullen and Evans BMC Ecol (2016) 16:52 Page 14 of 35 ‑ Ceratopsi dae 7 4 8 6 7 11 4 13 21 7 9 0 7 Eusuchia 27 28 53 36 54 7 24 59 30 25 123 33 13 - Champso saurus 7 15 109 41 14 7 4 25 26 7 91 68 55 Baenidae 16 5 6 10 14 0 8 3 12 7 30 5 1 ‑ Chelydri dae 3 2 5 4 3 3 0 5 11 4 21 3 1 Adocus 0 0 0 0 0 0 0 0 0 0 0 0 0 ‑ Trionychi dae 25 15 12 9 38 4 5 31 10 12 28 1 29 Basilemys 0 2 0 0 0 0 0 0 0 0 0 0 0 Solemydidae 0 0 0 0 0 0 0 0 0 0 0 0 0 ‑ Tes tudines indet. 0 0 0 0 0 0 0 0 0 0 0 0 0 ‑ Plesiosau ria 0 0 0 0 0 0 0 0 0 0 0 0 0 Squamata 7 11 12 17 9 5 3 22 27 12 61 25 13 Mosasauri ‑ dae 0 0 0 0 0 0 0 0 0 0 0 0 0 Caudata + Caudata ‑ Allocau data 45 47 347 283 125 120 64 194 340 266 550 235 178 continued pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) (DPF/ pre-LCZ; DPP) (DPF/ pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) (DPF/ pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) (DPF/ pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) BB94 (DPF/ BB75 (DPF/ BB54 (DPF/ BB120 BB106 BB25 (DPF/ BB117 BB78 (DPF/ BB104 BB97 (DPF/ BB86 (DPF/ BB51 (DPF/ BB31 (DPF/ 1 Table Taxon Cullen and Evans BMC Ecol (2016) 16:52 Page 15 of 35 ‑ Ceratopsi dae 3 0 9 0 0 1 4 0 6 10 5 15 Eusuchia 5 21 29 32 61 7 15 31 30 21 1 20 - Champso saurus 24 24 33 16 8 2 6 13 10 6 0 7 Baenidae 0 24 4 0 3 4 1 2 2 5 2 4 ‑ Chelydri dae 1 0 2 3 0 0 0 12 2 0 12 3 Adocus 0 0 0 0 0 0 0 0 0 0 0 0 ‑ Trionychi dae 15 7 12 15 19 5 12 14 3 3 6 1 Basilemys 0 0 0 0 0 0 0 0 0 0 0 0 Solemydidae 0 0 0 0 0 0 0 0 0 0 0 0 ‑ Tes tudines indet. 0 0 0 0 0 0 0 0 0 0 0 0 ‑ Plesiosau ria 0 0 0 0 0 0 0 0 0 0 0 0 Squamata 5 14 18 46 7 2 5 35 8 9 9 5 Mosasauri ‑ dae 0 0 0 0 0 0 0 0 0 0 0 0 Caudata + Caudata ‑ Allocau data 148 166 296 322 93 33 68 592 39 474 59 105 continued pre-LCZ; pre-LCZ; DPP) (OM/ Comrey; DPP) (OM/ Comrey; DPP) (OM/ Comrey; DPP) (OM/ Comrey; DPP) Comrey; DPP) (OM/ Comrey; DPP) (OM/ Comrey; DPP) upper; MRM) upper; MRM) upper; MRM) upper; MRM) BB98 (DPF/ BB107 BB100 BB103 BB121 BB71 (OM/ BB118 BB105 PLS (OM/ HAS (OM/ BMC (OM/ SalS (OM/ 1 Table Taxon Cullen and Evans BMC Ecol (2016) 16:52 Page 16 of 35 ‑ Ceratopsi dae 10 12 19 18 2 17 5 2 11 10 8 3 2 2 Eusuchia 93 82 118 11 5 21 4 51 13 20 82 31 38 51 - Champso saurus 37 14 9 1 2 2 4 27 6 18 214 17 50 28 Baenidae 16 6 14 5 8 6 10 13 1 4 11 2 18 8 ‑ Chelydri dae 15 1 10 9 15 6 23 0 2 0 5 14 4 1 Adocus 7 0 0 0 0 0 0 15 4 0 8 13 0 9 ‑ Trionychi dae 18 14 14 6 4 17 12 24 6 2 14 2 1 24 Basilemys 0 0 0 0 0 0 0 0 0 0 0 0 0 2 Solemydidae 0 0 0 0 0 0 0 0 0 0 0 0 0 35 ‑ Tes tudines indet. 0 0 0 0 0 0 0 0 0 0 0 0 0 3 ‑ Plesiosau ria 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Squamata 18 27 7 11 8 11 9 25 60 11 45 8 7 5 Mosasauri ‑ dae 0 0 0 0 0 0 0 0 0 0 0 0 0 1 Caudata + Caudata ‑ Allocau data 378 393 80 425 84 158 284 73 82 223 317 250 409 1 - continued - upper; MRM) upper; MRM) upper; MRM) upper; MRM) upper; MRM) upper; MRM) Comrey; MRM) lower; MRM) lower; MRM) (OM/ lower; MRM) lower; MRM) lower; MRM) most; MRM) most; MRM) CS (OM/ HS (OM/ RDS (OM/ CN-1 (OM/ CN-2 (OM/ CBC (OM/ ORS (OM/ PHS (OM/ EZ (OM/ PHR93-2 WS (OM/ HoS (OM/ SPS (Fore PK (Fore 1 Table Taxon Cullen and Evans BMC Ecol (2016) 16:52 Page 17 of 35 Mammalia 0 1 1 0 3 36 11 10 8 ‑ Ceratopsi dae 52 12 4 cf. Aves cf. 0 1 0 0 0 0 0 0 0 Eusuchia 122 205 151 - ‑ Tyrannosau ridae 0 0 1 2 4 2 1 1 0 Champso saurus 97 213 64 - Baenidae 93 2 2 Paronycho don 0 0 0 0 0 0 0 0 0 ‑ Chelydri dae 21 1 0 Troodon 0 0 0 0 2 3 0 0 0 - Adocus 129 3 15 Richardoes tesia 0 0 0 0 0 0 0 0 0 ‑ Trionychi dae 106 7 21 ‑ Saurorni tholestinae 0 0 0 2 35 47 7 0 8 Basilemys 0 0 0 ‑ Dromaeosau ridae 0 0 1 0 0 1 1 1 1 Solemydidae 1 0 272 ‑ Tes tudines indet. 0 0 0 Theropoda Theropoda indet. 0 0 0 0 0 0 0 0 0 ‑ Plesiosau ria 0 0 0 ‑ Hadrosauri dae 0 0 21 56 110 276 93 81 13 ‑ Squamata 12 11 0 Hypsilopho dont 0 0 0 0 0 0 0 0 0 Mosasauri ‑ dae 0 0 0 Ankylosauria 0 0 1 0 38 126 3 3 1 Caudata + Caudata ‑ Allocau data 41 103 24 continued - - - LCZ; DPP) LCZ; LCZ; DPP) LCZ; pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) (Fore most; MRM) (Fore most; MRM) (Fore most; MRM) BB96 (DPF/ L2377 (DPF/ BB115 (DPF/ BB119 (DPF/ BB108 (DPF/ BB102 (DPF/ BB94 (DPF/ BB75 (DPF/ BB54 (DPF/ PHR-1 PHR-2 PHRN 1 Table Taxon Taxon Site Cullen and Evans BMC Ecol (2016) 16:52 Page 18 of 35 Mammalia 24 1 3 2 0 15 2 9 7 8 7 7 4 16 cf. Aves cf. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ‑ Tyrannosau ridae 3 1 3 1 1 1 3 1 0 5 1 2 3 5 - Paronycho don 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Troodon 0 1 0 0 1 1 0 4 0 0 0 1 0 3 - Richardoes tesia 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ‑ Saurorni tholestinae 1 8 4 6 8 17 7 43 9 21 8 1 17 4 ‑ Dromaeosau ridae 0 2 1 0 1 1 1 2 2 1 0 0 0 3 Theropoda Theropoda indet. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ‑ Hadrosauri dae 113 100 73 67 174 186 121 424 116 104 106 65 161 263 ‑ Hypsilopho dont 0 0 0 0 0 0 2 4 3 3 0 1 1 2 Ankylosauria 3 25 6 13 8 14 5 76 12 11 6 75 69 342 continued pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) pre-LCZ; pre-LCZ; DPP) Comrey; DPP) Comrey; DPP) Comrey; DPP) BB120 (DPF/ BB106 (DPF/ BB25 (DPF/ BB117 (DPF/ BB78 (DPF/ BB104 (DPF/ BB97 (DPF/ BB86 (DPF/ BB51 (DPF/ BB31 (DPF/ BB98 (DPF/ BB107 (OM/ BB100 (OM/ BB103 (OM/ 1 Table Taxon Cullen and Evans BMC Ecol (2016) 16:52 Page 19 of 35 Mammalia 2 1 1 26 6 13 19 6 9 7 6 8 5 12 cf. Aves cf. 0 0 0 0 1 2 0 0 2 4 2 2 1 0 ‑ Tyrannosau ridae 1 0 0 3 3 3 4 2 4 1 4 3 1 3 - Paronycho don 0 0 0 0 2 2 1 1 1 3 0 0 1 0 Troodon 1 2 1 3 2 0 0 0 1 0 12 2 1 4 - Richardoes tesia 0 0 0 0 1 2 0 0 2 2 7 0 2 3 ‑ Saurorni tholestinae 6 2 7 28 25 8 4 5 6 4 41 10 1 7 ‑ Dromaeosau ridae 0 0 0 1 0 1 0 0 0 0 2 0 0 0 Theropoda Theropoda indet. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ‑ Hadrosauri dae 92 26 62 418 128 268 54 132 219 108 295 136 50 87 ‑ Hypsilopho dont 0 0 0 4 1 0 3 0 2 1 2 0 0 0 Ankylosauria 13 3 8 11 10 5 1 1 5 2 6 0 1 1 continued Comrey; DPP) Comrey; DPP) Comrey; DPP) Comrey; DPP) upper; MRM) upper; MRM) upper; MRM) upper; MRM) upper; MRM) upper; MRM) upper; MRM) upper; MRM) upper; MRM) upper; MRM) BB121 (OM/ BB71 (OM/ BB118 (OM/ BB105 (OM/ PLS (OM/ HAS (OM/ BMC (OM/ SalS (OM/ CS (OM/ HS (OM/ RDS (OM/ CN-1 (OM/ CN-2 (OM/ CBC (OM/ 1 Table Taxon Cullen and Evans BMC Ecol (2016) 16:52 Page 20 of 35 Mammalia 8 9 4 3 8 7 38 0 11 9 2 cf. Aves cf. 3 0 1 1 3 0 3 0 3 0 1 ‑ Tyrannosau ridae 1 2 1 0 3 2 1 1 7 9 1 - Paronycho don 1 1 0 1 2 0 2 0 0 1 0 Troodon 0 0 0 0 0 0 0 0 0 0 0 - Richardoes tesia 2 0 0 0 0 2 0 0 3 3 1 ‑ Saurorni tholestinae 1 7 1 11 7 6 2 4 7 18 0 ‑ Dromaeosau ridae 1 0 0 0 0 0 0 0 0 0 0 Theropoda Theropoda indet. 0 0 0 0 0 0 0 0 0 0 5 ‑ Hadrosauri dae 99 93 101 65 61 83 162 6 178 263 6 ‑ Hypsilopho dont 0 0 1 0 1 0 2 1 2 0 0 Ankylosauria 5 2 1 0 0 2 2 6 8 8 8 - continued Comrey; MRM) lower; MRM) lower; MRM) (OM/lower; MRM) lower; MRM) lower; MRM) most; MRM) MRM) (Foremost; (Foremost; MRM) (Foremost; (Foremost; MRM) (Foremost; (Foremost; MRM) ORS (OM/ PHS (OM/ EZ (OM/ PHR93-2 WS (OM/ HoS (OM/ SPS (Fore PK (Foremost; PK (Foremost; PHR-1 PHR-2 PHRN 1 Table Taxon Cullen and Evans BMC Ecol (2016) 16:52 Page 21 of 35

separation between the sampling localities is relatively (‘PHR-1’, ‘PHR-2’, ‘PHRN’) and both Lethbridge Coal small in the context of latitudinal climate gradients Zone sites (‘BB96’, ‘L2377’). The grade of sites (green (~150 km apart, with Dinosaur Provincial Park at ~50.75° highlighted component) situated between the two pri- latitude and Milk River at ~49.15° latitude), it is of a simi- mary clusters contains one Foremost Formation site lar magnitude to previous analyses of vertebrate end- (‘PK’) and four of the stratigraphically highest pre-LCZ emism in microsites [8, 14–16, 53, 58] and endemism/ Dinosaur Park Formation sites (‘BB102’, ‘BB119’, ‘BB108’, provinciality of large dinosaur macrofossils [1, 5, 19, 20, ‘BB115’). These stratigraphically high pre-LCZ Dinosaur 37, 43, 44]. The environmental matrix and the dissimilar- Park Formation sites (along with ‘BB94’, ‘BB75’, ‘BB54’, and ity matrix generated for the cluster analyses were then ‘BB120’, situated in the yellow highlighted component of ordinated via redundancy analysis (RDA) in order to Fig. 2) are positioned near the locally-variable conform- assess the relationship between each environmental vari- able boundary between the informal lower ‘sandy’ and able and the clustering of site faunal assemblages. upper ‘muddy’ units within the pre-LCZ Dinosaur Park Formation, a transition thought to indicate the accelera- Pair‑wise site assemblage similarity tion of the transgressive sequence leading into the LCZ Relative abundance data of site faunal assemblages were and Bearpaw Formation [12, 50, 52]. The two primary site split into two smaller datasets corresponding to sampling clusters correspond broadly to the clustering of taxa in location (DPP vs. MRM), and ordered stratigraphically. the R-mode analysis, with the larger site cluster associ- The proportions of each taxonomic group were then ated (yellow in Fig. 2) most strongly with lissamphibians plotted and compared using the R packages ‘ggplot2’ and (e.g. Caudata + Allocaudata), dinosaurs (e.g. Hadro- ‘reshape2’ [67, 68]. Additionally, pair-wise Bray-Curtis sauridae, Ceratopsidae, Troodon, Dromaeosauridae, cf. similarity values were computed for sites from each sam- Aves), and actinopterygians (e.g. ‘Holostean A’, Coriops, pling area using the ‘fossil’ package [69], and plotted as Teleostei, Esocidae), and the smaller primary site cluster curves showing relative changes in site similarity through (blue in Fig. 2) most strongly associated with batoids (e.g. stratigraphy. Average faunal proportions for each strati- Myledaphus + Pseudomyledaphus, Ischyrhiza, Protoplat- graphic interval were also produced and plotted. yrhina, Rhinobatos), sharks (e.g. Hybodus, Archaeolamna, This was repeated in three sub-sampling analyses Odontaspidae), and actinopterygians (e.g. Belonostomus, focused on the time-equivalent upper Oldman and Dino- Enchodus, Phyllodontidae). The sub-clusters within the saur Park formations, one including only dinosaur pro- larger (yellow in Fig. 2) of the two primary clusters are portions, another including only theropod proportions, broadly similar in taxonomic composition, with the only and one including non-dinosaur proportions. As with the major difference being the lack of several taxa (e.g. Paro- R- vs. Q-mode subsamples, the first two sub-sample anal- nychodon, Richardoestesia, cf. Aves) in Dinosaur Pro- yses used the re-sampled dataset of Dinosaur Provincial vincial Park sites. The grade of sites (green in Fig. 2) not Park sites (from Brinkman et al. [8]), for the same pur- included in the two primary clusters is associated with pose of more specific dinosaur taxon comparability, while aquatic taxa present to varying degrees in both other the third sub-sample used the primary dataset (with clusters (e.g. Myledaphus + Pseudomyledaphus, Lepisos- dinosaurs removed). teus, Eusuchia, Baenidae, Champsosaurus).

Results Redundancy analysis R‑ vs. Q‑mode cluster analysis Redundancy analysis (RDA) was carried out on the Cluster analyses of sites (Q-mode) and taxa (R-mode) percent difference dissimilarity matrix computed were performed and compared to identify major cluster- from the Belly River Group microsite relative abun- ing trends among Belly River Group microsites (Fig. 2). dance dataset, with stratigraphic interval (a proxy for Two primary site clusters were identified, with an addi- temporal change), depositional setting (site-specific tional grade of sites between them. The largest site clus- sedimentological characteristics), palaeogeographic ter (yellow highlighted component in Fig. 2) contains all sampling location (DPP or MRM), and palaeoenvi- Oldman Formation sites (N = 23), along with a majority ronment (as reconstructed for the broader area or of the pre-LCZ Dinosaur Park Formation sites (N = 14, interval within the geological formation) as explana- out of a possible 18), and one Foremost Formation site tory factors (Fig. 3). Broad overlap exists in sites pre- (‘SPS’). This cluster contains two large sub-clusters, served as crevasse splays or in-channel deposits, with which broadly group sites based on their sampling region these two representing the depositional setting of the (either DPP or MRM). The second primary site clus- vast majority of sites (Fig. 3a, red and green polygons), ter (blue highlighted component in Fig. 2) contains the though sites preserved as shoreface deposits did clus- three stratigraphically lowest Foremost Formation sites ter separately from other sites (Fig. 3a, blue polygon). Cullen and Evans BMC Ecol (2016) 16:52 Page 22 of 35

20 km Red Deer River a N

Dinosaur Provincial

BB102 BB103 BB121 Park BB54 BB105 BB98 BB96 BB94 BB71 BB78 BB107 L2377 BB97

BB108 BB117 BB115 BB100 BB106 BB104 BB120

BB118 BB119 Bow River BB75 2 km BB51 BB25 BB86 BB31 Medicine Hat

SPS

Oldman River

PK RDS CBC CS HS Alberta PHR-2 PHR93-2 PHRN ORS Milk River PHR-1 CN-2 CN-1 HAS PLS EZ PHS HoS WS SalS BMC

Dinosaur Lethbridge Coal Zone Lethbridge Coal Zone BB96, L2377 Park Fm. BB115 BB119 ‘muddy unit’ b BB108, BB102, BB94, BB75, Dinosaur BB54, BB120 Time-equivalent section: BB106 PLS Dinosaur Park Fm. (pre-LCZ) Park Fm. upper unit HAS & Oldman Fm. (upper unit) BMC BB25, BB117, BB78 ‘sandy unit’ BB104 Sal S BB97 CS, HS, RDS, CN-1, CN-2 CBC BB86, BB51, BB31, BB98 Oldman BB107 Fm. BB100, BB103, BB121 middle unit / ORS Oldman middle unit / Comrey ss BB71, BB118 Comrey ss Fm. BB105

lower unit

PHS lower unit EZ PHR93-2

Belly River Group WS, HoS

Taber Coal Zone + Unit 2 Dinosaur Provincial Park SPS, PK PHR-1, PHR-2 Localities Foremost PHRN Fm. Unit 1

Cretaceous (Campanian) Milk River / Manyberries Localities Fig. 1 Locality map of Belly River Group sites analyzed in this study. a Geographic location of sites in Alberta, in context to regional landmarks; b relative stratigraphic positions of sites within the Belly River Group at each sampling region. Map modified from [16] and site locality data compiled from [12, 14, 16]

Palaeogeographic sampling location was effective at Oldman and pre-LCZ Dinosaur Park formations separating site clusters in certain situations, such as (Fig. 3b, dark red and blue polygons). When expanded for sites in the time-equivalent portion of the upper to all sites, sampling location did not produce distinct Cullen and Evans BMC Ecol (2016) 16:52 Page 23 of 35

BMC (OM/upper) PLS (OM/upper) RDS (OM/upper) SalS (OM/upper) CBC (OM/upper) CN−2 (OM/upper) HAS (OM/upper) ORS (OM/Comrey) HS (OM/upper) CS (OM/upper) EZ (OM/lower) CN−1 (OM/upper) PHR93−2 (OM/lower) WS (OM/lower) BB103 (OM/Comrey) BB107 (OM/Comrey) BB105 (OM/Comrey) BB118 (OM/Comrey) BB31 (DPF/pre-LCZ) BB100 (OM/Comrey) BB98 (DPF/pre-LCZ) BB104 (DPF/pre-LCZ) BB97 (DPF/pre-LCZ) BB86 (DPF/pre-LCZ) BB25 (DPF/pre-LCZ) BB78 (DPF/pre-LCZ) BB106 (DPF/pre-LCZ) BB51 (DPF/pre-LCZ) BB71 (OM/Comrey) BB121 (OM/Comrey) BB117 (DPF/pre-LCZ) BB120 (DPF/pre-LCZ) BB94 (DPF/pre-LCZ) BB75 (DPF/pre-LCZ) HoS (OM/lower) PHS (OM/lower) BB54 (DPF/pre-LCZ) SPS (For) BB102 (DPF/pre-LCZ) BB119 (DPF/pre-LCZ) BB108 (DPF/pre-LCZ) BB115 (DPF/pre-LCZ) PK (For) PHR−1 (For) PHR−2 (For) PHRN (For) BB96 (DPF/LCZ) L2377 (DPF/LCZ) Theropoda indet . Centrophoroides Synechodus Elasmobranchii indet . Cretolamna Orectolobidae Squatina Protoplatyrhin a Odontaspidida e Rhinobatos Elasmodu s Plesiosauria Enchodus Archaeolamna Ischyrhiz a Hybodu s Mosasauridae Solemydida e Testudines indet . Basilemy s Adocus Paratarpon Chiloscylliu m ‘Holostean B’ Phyllodontidae Myledaphus + Pseudomyledaphu s Acipenseriformes Belonostomus Dromaeosauridae Ankylosauria Lepisosteus Trionychida e Eusuchia Baenidae Champsosaurus Squamata Saurornitholestina e ‘Holostean A’ Coriops Teleostei indet. Hadrosauridae Caudata + Allocaudat a Esocidae Ceratopsidae Anur a Amiidae Tyrannosauridae Mammalia Chelydrida e Hypsilophodont Troodo n Richardoestesi a cf. Aves Paronychodon

Fig. 2 R-mode vs. Q-mode cluster analysis of Belly River vertebrate microfossil sites. Dinosaur Provincial Park sites indicated with blue text and trian- gles. Milk River/Manyberries sites indicated with red text and circles. Coloured regions note environments associated with indicated sites and taxa: yellow terrestrial, green transitional, blue marine Cullen and Evans BMC Ecol (2016) 16:52 Page 24 of 35

clusters, and broad overlap was found relating to the Pair‑wise site assemblage similarity position of lower Belly River Group sites from Milk Pair-wise Bray-Curtis (percentage-difference) similarity River and upper Belly River Group sites from DPP was computed for each consecutive pair of stratigraph- (Fig. 3b, light red and blue polygons). When the strati- ically-ordered neighbouring sites from each sampling graphic interval of each site was analyzed as a cluster- region (DPP and MRM), along with a visual representa- ing variable, considerable overlap was found and no tion of relative taxonomic group abundance at each site directional organization could be found that would (Fig. 4). The Milk River/Manyberries sites (Fig. 4, red box be consistent with a linear relationship through time at right) range stratigraphically from the Foremost For- (Fig. 3c). Sites from the lower and middle (Comrey mation to the upper unit of the Oldman Formation (time- sandstone) Oldman Formation (Fig. 3c, purple and equivalent to the pre-LCZ Dinosaur Park Formation in yellow polygons) plotted adjacent to one another, DPP), and the Dinosaur Provincial Park sites (Fig. 4, blue with a broad overlapping distribution of sites from box at left) stratigraphically range from the middle Old- the upper Oldman and pre-LCZ Dinosaur Park for- man Formation (‘Comrey sandstone’) to the Lethbridge mations (Fig. 3c, green polygon). Most Foremost For- Coal Zone. Pair-wise similarity curves are relatively sta- mation sites (Fig. 3c, blue polygon) plotted between ble for much of the sampled intervals in both DPP (Fig. 4, pre-LCZ Dinosaur Park Formation sites from high in blue curve) and MRM (Fig. 4, red curve), ranging from stratigraphic section (Fig. 3c, sites of green polygon approximately 50–80% similarity. Two exceptions to this with more negative positions on first RDA axis), near stability exist, one during the regressive phase recorded the boundary with the LCZ, and sites from within the near the end of the Foremost Formation in MRM sites Lethbridge Coal Zone itself (Fig. 3c, light blue poly- (Fig. 4, near base of red curve) and the other during the gon). The exception to this was the ‘SPS’ site, which transgressive phase in the Lethbridge Coal Zone near the plotted most closely to lower Oldman Formation sites. boundary between the Belly River Group and the overly- When using palaeoenvironment as a factor, sites were ing Bearpaw Formation in DPP sites (Fig. 4, near top of assigned to one of four settings, based on their lithol- blue curve). In both of these cases, site similarity dropped ogy and predominant fauna: (1) marine, (2) transi- to approximately 10–20%. Trends recorded across rela- tional, (3) terrestrial (paralic; lower coastal plain), tive abundances of taxa in individual sites (Fig. 4, DPP and (4) terrestrial (alluvial; upper coastal plain). The sites in blue box at left and MRM sites in red box at right) two terrestrial groupings correspond to the palaeoen- and in formational average taxon abundance (Fig. 4, top vironmental conditions from which the vast majority right) both show that the site similarity drop in the Fore- of dinosaur fossils are known, and represent the two most Formation was associated with large reductions primary environmental regimes discussed in previ- in relative abundances of chondrichthyans and large ous studies of dinosaur environmental sensitivity and/ increases in relative abundances of lissamphibians, with or provinciality/endemism [1–7, 9, 19, 20, 22–25, 36, the inverse seen in the similarity drop in the Lethbridge 37, 42–45, 49, 70]. Three non-overlapping grouping Coal Zone. were obtained: one for sites with palaeoenvironments reconstructed as marine (Fig. 3d, blue polygon), one Sub‑sample analyses of time‑equivalent sites for sites reconstructed as transitional and preserving a Using three subsets of the broader relative abundance mix of marine and terrestrial sedimentological features dataset, with re-sampled values of dinosaurs from Brink- and taxa (Fig. 3d, purple polygon), and a final group- man et al. [8] in place of Brinkman [12] for the first two, ing for sites reconstructed as being terrestrial (Fig. 3d, R- vs. Q-mode cluster analyses and pair-wise assem- green and yellow polygons). Sites with terrestrial blage similarity analyses were performed for dinosaur- palaeoenvironments were further subdivided based only (Fig. 5), theropod-only (Fig. 6), and non-dinosaur on their prior associations with more paralic, lower (Fig. 7) components of the assemblage. These subset coastal plains (Fig. 3d, green polygon) or more alluvial, comparisons were made only for sites in the overlapping upper coastal plains (Fig. 3d, yellow polygon). These stratigraphic intervals of each sampling area, namely the further subdivisions followed a clustering pattern con- middle (‘Comrey sandstone’) Oldman Formation, and the sistent with other sites, with more inland terrestrial upper Oldman Formation and pre-LCZ Dinosaur Park sites plotting further from marine and transitional Formation. sites than more coastal plain terrestrial sites. Despite In the dinosaur sub-sample (Fig. 5), hadrosaurs consti- this trend, considerable overlap exists between more tuted the vast majority of assemblage relative abundance coastally influenced terrestrial sites and more alluvial in almost all sites from both Dinosaur Provincial Park and terrestrial sites, indicating that the two cannot be con- Milk River. The only exception to this was the DPP ‘BB54’ sidered truly distinct for the purpose of site clustering. site, which clustered away from all other sites (Fig. 5A). Cullen and Evans BMC Ecol (2016) 16:52 Page 25 of 35

a Depositional Setting b Palaeogeography 1.0 1.0

BB54 BB71 BB103 BB54 BB71 BB103 BB75 BB75 BB121 BB107 BB121 BB107 BB51 BB51 BB94 BB106 BB31 BB94 BB106 BB31 0.5 BB100 BB118 0.5 BB100 BB118 BB105 BB105 BB115 BB78 BB115 BB78 BB120 BB86 BB98 BB120 BB86 BB98 BB102 BB104 BB102 BB104 BB25 BB97 BB25 BB97 BB117 BB117 BB119 HoS BB119 HoS PHS PHS PHR−1 BB108 PHR−1 BB108 PK PK 0.0 0.0 WS WS PHR93−2 PHR93−2 SPS SPS SalS SalS EZ EZ

CS HAS CS HAS

CBC CN−1 CBC CN−1 PHR−2 RDS PHR−2 RDS −0.5 −0.5

ORS ORS HS HS

BB96 PLS BB96 PLS PHRN BMC PHRN BMC −1.0 −1.0

CN−2 CN−2

Northern / Dinosaur Provincial Park Sites (time-equivalent upper Oldman & pre-LCZ Dinosaur Park fms only) L2377 L2377 Northern / Dinosaur Provincial Park Sites (all lithostratigraphic units) −1.5 Shoreface Deposit −1.5 Southern / Milk River Sites Crevasse Splay Deposit (time-equivalent upper Oldman & pre-LCZ Dinosaur Park fms only) In-Channel Deposit Southern / Milk River Sites (all lithostratigraphic units)

−1.5 −1.0 −0.5 0.0 0.5 −1.5 −1.0−0.5 0.0 0.5 RDA1 RDA1

c Stratigraphic Interval d Palaeoenvironmental Setting .0 1.0

BB54 BB71 BB103 BB54 BB71 BB103 BB75 BB75 BB121 BB107 BB12121 BB107B BB51 BBBB51 BB94 BB106 BB31 BB9494 BB10B 6 BBBB313 0. 51 BB100 BB118 0.5 BBBB101000 BBBB111 8 BB105 BB105 BB115 BB78 BB115 BB102 BBB78 BB120 BB86 BB98 BBBB12120 BB86 BBBB98998 BB102 BB104 BB10B 4 BB25 BB97 BBBB25B225 BBBB9797 BB117 BBBBB111117 HoS HoS BB119 BB119 PHS PHP S PHR−1 BB108 PHR−1 BB108 .0 PK .0 PK WS WSS PHR93−2 PHR9PHR93−3−3 2 SPS SPS SalS SSalS EZ EZ

CS HAS CS HAS

CBC CN−1 CCBBC CN−1 PHR−2 PHR−2

0. 50 RDS RDS −0. 50

ORS ORS HS HS

BB96 PLS BB96 PLS PHRN BMC PHRN BMC −1. 0− −1.0

CN−2 CN−2N

Dinosaur Park Fm. (Lethbridge Coal Zone) L2377 Oldman Fm. (upper unit) / Dinosaur Park Fm. (pre-LCZ) L2377 Terrestrial Sites (Alluvial / Upper Coastal Plain) Oldman Fm. (middle unit) −1.5 −1.5 Terrestrial Sites (Paralic / Lower Coastal Plain) Oldman Fm. (lower unit) Transitional Sites Foremost Fm. Marine Sites

−1.5 −1.0 −0.5 0.0 0.5 −1.5 −1.0−0.5 0.0 0.5 RDA1 RDA1 Fig. 3 Redundancy analysis of Belly River Group vertebrate microfossil site data and associated environmental factors. a Depositional setting; b palaeogeo- graphic sampling location; c stratigraphic interval; d palaeoenvironmental setting. Subdivisions within each environmental factor noted in associated legends Cullen and Evans BMC Ecol (2016) 16:52 Page 26 of 35

Pair-Wise Assemblage a Similarity Through Taxa by Site: Dinosaur Provincial Park (DPP) Lithostratigraphy Taxa by Site: Milk River / Manyberries (MRM)

Dinosaur BB96 Park Fm. Shorelin e L2377 (LCZ) Shorelin e BB115 BB119 Microsites currently BB108 BB102 unsampled from this BB94 interval in MRM BB75 BB54 Paralic / Lower Coastal Plai n BB120 BB106 PLS BB25 HAS (pre-LCZ) BB117 BMC Dinosaur Park Fm . BB78 Paralic / Lower Coastal Plai n SalS BB104 CS n BB97 i

a HS l P l (upper unit ) Oldman Fm .

BB86 a RDS t s a

BB51 o CN−1 C r

BB31 e CN−2 p p

BB98 U CBC / l a BB107 i v u l l

BB100 A BB103 BB121 ORS BB71 Oldman Fm . Oldman Fm . BB118 (middle unit / Comrey ss) (middle unit / Comrey ss)

BB105 Alluvial / Upper Coastal Plai n n i PHS a l P l

a EZ Percentagen (%) t s a

o PHR93−2 C r

e WS (lower unit ) w Microsites currently Oldman Fm . o

L HoS / c i unsampled from this l Foremost SPS a

r Fm. a

P (Unit 2) interval in DPP Paralic / Lower Coastal Plai n PK e n

i PHR−1 l

e Foremost r

o Fm. PHR−2 h (Unit 1) S Shorelin e PHRN

0255075 100 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 025750 5 100 Percentage (%) Percentage (%) Bray-Curtis Similarity

b Dinosaur Provincial Milk River / Manyberries Taxa Averages by Lithostratigraphic Unit LEGEND Park Pairwise Similarity Pairwise Similarity 100 Curve Curve

75 Batoidea Holostei Testudines Choristodera

50 Selachimorpha Teleostei Sauropterygia Crocodylomorpha 25 Percentage (%) Elasmobranchii Anura Squamata Dinosauria 0 (other/indet.) Foremost Fm. Foremost Fm. Oldman Fm. Oldman Fm. Oldman Fm. Dinosaur Park (Unit 1) (Unit 2) (lower unit) (middle unit / (upper unit) / Fm. (LCZ) Comrey ss) Dinosaur Park Fm Chondrostei Caudata + Allocaudata Mammalia (pre-LCZ) Fig. 4 a Pair-wise Bray-Curtis similarity of Dinosaur Provincial Park (blue square) and Milk River/Manyberries (red square) vertebrate microfossil rela- tive abundance assemblages through Belly River Group lithostratigraphic record. b Formational average proportions of each taxonomic group in sampled regions Taxonomic groups, site identifications, and other relevant information noted in legend

With the exception of hadrosaurs, no single dinosaur taxon represented by red similarity curve). The only deviation was found to be driving large-scale site clustering, though from this trend is a drop to approximately 20% similarity increased Troodon relative abundance seems to drive the for sites neighbouring ‘BB54’, which as noted above rep- finer-scale clustering of two MRM sites (‘RDS’ and ‘CBC’) resents an apparent outlier due to a lower relative abun- and a DPP site (‘BB71’), and relative abundance of anky- dance of hadrosaurs, and much higher relative abundances losaurs drives the clustering of two DPP sites (‘BB86’ and of ceratopsians and Richardoestesia (Fig. 5b). Formational ‘BB100’) and one MRM site (‘PLS’). Unlike in the cluster average abundances of dinosaurs (Fig. 5c) do not show any analyses of the broader vertebrate assemblages, there is major shifts in assemblage between the middle Oldman less distinct clustering of sites by sampling region (Fig. 5a, Formation sites and the sites of the time-equivalent upper MRM sites indicated by red circles and DPP sites indicated Oldman and pre-LCZ Dinosaur Park formations, nor is by blue triangles). Pair-wise site similarity for dinosaur there considerable difference in assemblages between assemblages in the sub-sampled interval is relatively stable the DPP and Milk River localities. The only exceptions for both DPP and MRM, ranging approximately 40–80% to this are a moderate increase in ceratopsians in DPP similarity (Fig. 5b, DPP sites in blue box and represented between the middle Oldman Formation (~1% relative by blue similarity curve and MRM sites in red box and abundance) and time-equivalent pre-LCZ Dinosaur Park Cullen and Evans BMC Ecol (2016) 16:52 Page 27 of 35

Formation (~7% relative abundance), a shift also found in (e.g. Basilemys, Baenidae, Trionychidae). Two sites, both the equivalent intervals of the Milk River sites (~4 to ~7% stratigraphically high in the DPF and close to the LCZ, relative abundance, respectively). In the middle Oldman were associated with batoids (e.g. Myledaphus + Pseudo- Formation and time-equivalent upper Oldman Formation myledaphus), Basilemys, and in one case sharks (Hybo- of Milk River, there were also changes in small theropod dus, in ‘BB115’). As in other analyses, ‘BB54’ grouped as relative abundances, with saurornitholestines increas- something of an outlier, and was here associated strongly ing slightly (~1 to ~5%), and Troodon going from absent with ‘Holostean A’ and ‘Holostean B’. Other DPP sites to present (with relative abundance in the upper Oldman were broadly associated with many taxa, though in par- Formation of ~1%). ticular with actinopterygians (e.g. Coriops, ‘Holostean A’), The theropod-only sub-sample analyses (Fig. 6) pro- baenid turtles, and lissamphibians (e.g. Caudata + Allo- duced similar results to the sub-sample of dinosaurs. caudata). Sites sampled from MRM as a whole were dis- Most sites did not show any strong signal from a par- tinguished from DPP mainly due to an even stronger ticular taxon driving clustering patterns (Fig. 6a), though association with lissamphibians (e.g. Caudata + Allocau- a few clustered together due to their greater associa- data) and certain actinopterygians (e.g. esocids, teleosts), tion with tyrannosaurids and Richardoestesia (‘BB120’, though particular MRM sites were also distinguished ‘BB115’, ‘BB75’, BB119) or with cf. Aves (‘BB61’, ‘CN-2’, based on their association with taxa that were either ‘ORS’, ‘HS’). As with dinosaurs, the site similarity curves absent or in low abundance at other sites, particularly of the theropod sub-samples from DPP and MRM are those from DPP. For example, Adocus and Chiloscyllium very similar (Fig. 6b), both staying within a range of ~30 are strongly associated with the ‘CS’ site, though absent to ~80% similarity. The lower bound of that similarity or in very low abundance in most sites. One MRM site range related to sites neighbouring those with very lit- (‘BMC’) clustered as an outlier, and was distinguished tle theropod material (e.g. ‘BB120’, ‘BB75’, ‘BB115’, and through a suite of taxa (e.g. chelydrid turtles, mammals, ‘BB119’). The formational average theropod relative anurans, squamates). Both of these outlier sites (‘BB54’ abundances (Fig. 6c) in DPP show no appreciable differ- and ‘BMC’) have been noted in previous research to be ences, with slight increases in proportions of tyrannosau- sedimentologically distinct from other sites, possibly rids and Richardoestesia, and slight decrease in Troodon. representing an exception to the general trend of depo- In MRM, there are more considerable differences in for- sitional setting having a relatively small effect on micro- mational average relative theropod abundances, with sau- site assemblage structure [14, 52]. Site similarity curves rornitholestine proportions greatly increasing, Troodon for DPP and MRM (Fig. 7b) were very similar, and very appearing in the upper Oldman Formation while not stable, both fluctuating around 60% similarity for much being found in the middle Oldman Formation, and all of the sampled interval. The only prominent exception other taxa proportionally decreasing slightly. to this came at the top of the time-equivalent interval in The non-dinosaur sub-sample analysis (Fig. 7) pro- DPP, where similarity began to steadily drop, reaching duced similar results to the non-marine components of approximately 40% similarity by the top of the sampled the R- vs. Q-mode analysis of all microsite data (Fig. 2, interval. Overall proportions of major taxonomic groups yellow square). Clustering of sites based on their prove- in DPP and MRM during this interval (Fig. 7c) were simi- nience was apparent, though sites did not cluster exclu- lar, with the notable exception being the higher propor- sively based on being from DPP or MRM (Fig. 7a). Sites tion of batoids in DPP (<20%) when compared to MRM from MRM clustered more closely to the majority of DPP (<5%). sites than a number of DPP sites (e.g. ‘BB106’, ‘BB117’, ‘BB121’, ‘BB94’, ‘BB75’, ‘BB119’, ‘BB102’), with those latter Discussion sites forming a cluster more similar to each other than Drivers of faunal assemblage clustering in the Belly River to any other site. This cluster was associated the propor- Group tion of particular actinopterygians (e.g. Lepisosteus, Par- Our results broadly support the conclusions of previ- atarpon, Acipenseriformes, Belonostomus), and turtles ous studies such as Brinkman et al. [14], expand on their

(See figure on next page.) Fig. 5 a R-mode vs. Q-mode cluster analysis of dinosaur component of Belly River Group microsites from the time-equivalent interval of the Old- man and Dinosaur Park formations of Dinosaur Provincial Park and Milk River/Manyberries. Dinosaur Provincial Park sites indicated with blue text and triangles. Milk River/Manyberries sites indicated with red text and circles. b Pair-wise Bray-Curtis similarity of Dinosaur Provincial Park (blue square) and Milk River/Manyberries (red square) microsite dinosaur relative abundance assemblages through lithostratigraphic record of time-equivalent Oldman and Dinosaur Park formations. c Formational average proportions of each dinosaur group in sampled regions. Taxonomic groups, site identifications, and other relevant information noted in legend Cullen and Evans BMC Ecol (2016) 16:52 Page 28 of 35

a

Troodon

Saurornitholestinae

Tyrannosauridae

Ceratopsidae

Hadrosauridae

Ankylosauria

Hypsilophodont

cf. Aves

Richardoestesia

Paronychodon

Dromaeosauridae CS (OM/upper ) HS (OM/upper ) PLS (OM/upper ) HAS (OM/upper ) RDS (OM/upper ) SalS (OM/upper ) CBC (OM/upper ) BMC (OM/upper ) CN−2 (OM/upper ) CN−1 (OM/upper) BB71 (OM/Comrey ) ORS (OM/Comrey ) BB25 (DPF/pre-LCZ ) BB98 (DPF/pre-LCZ ) BB75 (DPF/pre-LCZ ) BB97 (DPF/pre-LCZ ) BB94 (DPF/pre-LCZ ) BB78 (DPF/pre-LCZ ) BB86 (DPF/pre-LCZ ) BB51 (DPF/pre-LCZ ) BB31 (DPF/pre-LCZ ) BB54 (DPF/pre-LCZ ) BB118 (OM/Comrey ) BB107 (OM/Comrey ) BB103 (OM/Comrey ) BB105 (OM/Comrey ) BB121 (OM/Comrey ) BB100 (OM/Comrey ) BB108 (DPF/pre-LCZ ) BB117 (DPF/pre-LCZ ) BB102 (DPF/pre-LCZ ) BB120 (DPF/pre-LCZ ) BB115 (DPF/pre-LCZ ) BB106 (DPF/pre-LCZ ) BB119 (DPF/pre-LCZ ) BB104 (DPF/pre-LCZ ) b

Dinosaurs by Site: Pair-Wise Dinosaur Assemblage Dinosaurs by Site: Similarity Dinosaur Provincial Park Through Lithostratigraphy Milk River / Manyberries

BB115

BB119

BB108

BB102

BB94

BB75

BB54 Paralic / Lower Coastal Plain

BB120

BB106 PLS

BB25 HAS (pre-LCZ ) BB117 BMC Dinosaur Park Fm .

BB78 SalS Paralic / Lower Coastal Plain BB104 CS

BB97 HS (upper unit ) Oldman Fm . BB86 RDS

BB51 CN−1

BB31 CN−2

BB98 CBC

BB107 Alluvial / Upper Coastal Plain

BB100

BB103

BB121 ORS

BB71 Oldman Fm . Oldman Fm . BB118 (middle unit / Comrey ss ) (middle unit / Comrey ss ) BB105 Alluvial / Upper Coastal Plain

0255075100 0255075100 Percentage (%) 0.10.2 0.30.4 0.50.6 0.70.8 Percentage (%) c Bray-Curtis Similarity Taxa Averages by Lithostratigraphic Unit: Dinosaur Provincial Park 100 LEGEND 75 Dromaeosauridae 50 Ceratopsidae Saurornitholestinae 25 Ankylosauria Troodon 0 Oldman Fm. (middle unit / Comrey ss) Oldman Fm. (upper unit) / Dinosaur Park Fm. (pre-LCZ) Hypsilophodont Richardoestesia Taxa Averages by Lithostratigraphic Unit: Hadrosauridae Paronychodon Milk River / Manyberries Tyrannosauridae Aves indet. 100

75 Dinosaur Provincial Park SitesMilk River / Manyberries Sites

50 Dinosaur Provincial Park Milk River / Manyberries 25 Pairwise Similarity Curve Pairwise Similarity Curve

0 Oldman Fm. (middle unit / Comrey ss) Oldman Fm. (upper unit) / Dinosaur Park Fm. (pre-LCZ) Cullen and Evans BMC Ecol (2016) 16:52 Page 29 of 35

work to include sites from both MRM and DPP in a moderately abundant in MRM sites, despite these taxa series of analyses, and more thoroughly test the role that being reported in the Dinosaur Park Formation [71]. This various abiotic factors play in structuring the preserved effect is similarly seen in the PHRN site (Fig. 2) being faunal assemblages. The results of the R- vs. Q-mode associated with ‘Theropoda indet’ material (alongside cluster analyses (Fig. 2), RDA analyses (Fig. 3), and pair- the numerous marine chondrichthyan taxa that primarily wise site similarity comparisons (Fig. 4) for the full sam- characterize the site) due to this taxonomic category only ple of microsite faunal assemblages of MRM and DPP existing for this site (based on the source data). indicate that palaeoenvironmental changes, particularly Overall, the results of these analyses for the entire Belly marine-terrestrial transitions, are responsible for the River Group microsite database build on prior research most significant changes in faunal assemblage structure, conducted on this subject [8, 12–14, 16, 53, 58, 61], and and that other factors like site depositional setting, rela- serve to more thoroughly and quantitatively establish tive stratigraphic position within the Belly River Group, the patterns that have been observed in this system. It is and palaeogeographic sampling location played a lesser not particularly surprising that changes in sea level in the to negligible role. While depositional setting (Fig. 3a) Belly River Group acted as a strong driver of environmen- appears superficially to explain site clustering, it should tal and faunal assemblage change, as the most significant be noted that the only depositional setting that did not change in faunal assemblage during these intervals is the display considerable overlap with others were shore- inverse proportional change in chondrichthyans and lis- face deposits, and each site characterized as a shoreface samphibians, which is almost certainly related to the deposit was also characterized as preserving a primarily degree of marine preference (or lack-thereof in the latter marine palaeoenvironment. Of the three depositional case) in these taxa [16, 72, 73]. However, it is important to settings analyzed, there was broad overlap in sites charac- quantify and understand the exact nature of these trends, terized as crevasse splays or in-channel deposits (Fig. 3a), as these controvertial data form the baseline for future which is consistent with palaeoenvironment (Fig. 3d) comparisons and facilitate the testing of more controver- driving site clustering, as there is also considerable over- sial questions, such as the environmental sensitivity of lap in terrestrial sites, all of which in this sample are pre- dinosaurs and the effects that more subtle environmental served as either in-channel or crevasse splay deposits. variation have on local palaeocommunity structure. The differing depositional characteristics of these ter- restrial sites are therefore not having a strong effect on Altitudinal and latitudinal sensitivity of dinosaur the preserved faunal assemblage. Palaeogeographic sam- assemblages pling location appears to also have some effect on faunal The sensitivity of dinosaur populations to changes in alti- assemblage structure, at least within sites from the time- tudinal (distance from palaeoshoreline) and latitudinal equivalent interval of the Oldman and pre-LCZ Dino- environmental gradients has been the subject of consider- saur Park formations of Dinosaur Provincial Park and able debate for over 30 years [1–9, 11, 15, 23, 26, 27, 42–46, Milk River (Fig. 3b). In that context, the DPP and MRM 55, 62, 70], and although it has been questioned [17, 18, 22, sites formed distinct clusters, though this separation 28, 74], it remains one of the primary explanations for pat- did not hold when expanded to the complete sample of terns observed in the evolution and distribution of dino- Belly River Group microsites. The separate timeequiva- saurs throughout the Late Cretaceous of western North lent DPP and MRM clusters provide further support to America. A focused sub-sampling of the time-equivalent the hypothesis that at least some of the differences in interval of the Oldman and Dinosaur Park formations microsite faunal assemblage structure is the result of bio- within the larger Belly River Group microsite abundance geographic differences related to environmental variation dataset facilitates a controlled and direct test of dinosaur across the palaeolandscape [12, 14]. However, the distinct assemblage changes across differing palaeoenvironments clustering of these sites may also be an artefact related (Figs. 5, 6), while also allowing comparisons to the non- to the absence of several taxa (e.g. Paronychodon, cf. dinosaur component of the broader vertebrate assemblage Aves, Richardoestesia) in the DPP microsite data that are (Fig. 7) albeit at a regional, rather than continental, scale.

(See figure on next page.) Fig. 6 a R-mode vs. Q-mode cluster analysis of theropod component of Belly River Group microsites from the time-equivalent interval of the Old- man and Dinosaur Park formations of Dinosaur Provincial Park and Milk River/Manyberries. Dinosaur Provincial Park sites indicated with blue text and triangles. Milk River/Manyberries sites indicated with red text and circles. b Pair-wise Bray-Curtis similarity of Dinosaur Provincial Park (blue square) and Milk River/Manyberries (red square) microsite theropod relative abundance assemblages through lithostratigraphic record of time-equivalent Oldman and Dinosaur Park formations. c Formational average proportions of each theropod group in sampled regions. Taxonomic groups, site identifications, and other relevant information noted in legend Cullen and Evans BMC Ecol (2016) 16:52 Page 30 of 35

a

Dromaeosauridae

Tyrannosauridae

Richardoestesia

Troodon

Saurornitholestinae

Paronychodon

cf. Aves CS (OM/upper) HS (OM/upper) PLS (OM/upper ) HAS (OM/upper) RDS (OM/upper) SalS (OM/upper) CBC (OM/upper) BMC (OM/upper) CN−1 (OM/upper ) CN−2 (OM/upper ) BB71 (OM/Comrey) ORS (OM/Comrey ) BB75 (DPF/pre-LCZ ) BB98 (DPF/pre-LCZ ) BB97 (DPF/pre-LCZ ) BB25 (DPF/pre-LCZ ) BB86 (DPF/pre-LCZ ) BB78 (DPF/pre-LCZ ) BB94 (DPF/pre-LCZ ) BB31 (DPF/pre-LCZ ) BB51 (DPF/pre-LCZ ) BB54 (DPF/pre-LCZ ) BB118 (OM/Comrey ) BB103 (OM/Comrey ) BB121 (OM/Comrey) BB107 (OM/Comrey ) BB105 (OM/Comrey ) BB100 (OM/Comrey) BB120 (DPF/pre-LCZ ) BB115 (DPF/pre-LCZ) BB119 (DPF/pre-LCZ ) BB108 (DPF/pre-LCZ) BB117 (DPF/pre-LCZ ) BB102 (DPF/pre-LCZ) BB106 (DPF/pre-LCZ) BB104 (DPF/pre-LCZ) b

Theropods by Site: Pair-Wise Theropod Theropods by Site: Similarity Dinosaur Provincial Park Through Lithostratigraphy Milk River / Manyberries

BB115 n i a BB119 l P l a t

BB108 s a o C

BB102 r e w

BB94 o L / c i BB75 l n a i r a l a P BB54 P l a t s

BB120 a o C

BB106 r e PLS w o L

BB25 (pre-LCZ ) HAS / c i l Dinosaur Park Fm .

BB117 a BMC r a BB78 P SalS

BB104 CS n BB97 i HS (upper unit) a Oldman Fm . l P l

BB86 a RDS t s a

BB51 o CN−1 C r e

BB31 p CN−2 p U

BB98 / CBC l a i v u

BB107 l l n i A a l

BB100 P l a t s

BB103 a o C

r ORS

BB121 e p p U

BB71 Oldman Fm . / Oldman Fm . l a i

BB118 v u l (middle unit / Comrey ss ) l (middle unit / Comrey ss) BB105 A

0255075 100 0255075 100 Percentage (%) 0 0.2 0.4 0.60.8 1.0 Percentage (%) c Bray-Curtis Similarity Taxa Averages by Lithostratigraphic Unit: Dinosaur Provincial Park 100 75 LEGEND

50 Troodon Tyrannosauridae 25 Richardoestesia 0 Dromaeosauridae Oldman Fm. (middle unit / Comrey ss) Oldman Fm. (upper unit) / Paronychodon Dinosaur Park Fm. (pre-LCZ) Taxa Averages by Lithostratigraphic Unit: Saurornitholestinae Aves indet. Milk River / Manyberries 100 Dinosaur Provincial Park SitesMilk River / Manyberries Sites 75 Dinosaur Provincial Park Milk River / Manyberries 50 Pairwise Similarity Curve Pairwise Similarity Curve 25 0 Oldman Fm. (middle unit / Comrey ss) Oldman Fm. (upper unit) / Dinosaur Park Fm. (pre-LCZ) Cullen and Evans BMC Ecol (2016) 16:52 Page 31 of 35

Within dinosaurs (Fig. 5) there is broad assemblage sta- is more dynamic than originally described [50], though, bility, despite the sampled regions representing differing pending future geological investigations, there is currently terrestrial environments (lower coastal plain vs. upper no reason to think this is the case. The relative similar- coastal plain/inland alluvial fan). In both DPP and MRM, ity of the dinosaur faunal assemblages of DPP and MRM, hadrosaurs dominate the preserved dinosaur assemblages, and how those contrast to the differences seen in the rest often representing over 80% of relative abundance. A mod- of the vertebrate faunal assemblage between these areas erate increase in ceratopsians is noted through time in and throughout the extent of the Belly River Group, does DPP, though across time-equivalent intervals the propor- not support the idea that dinosaurs, including large bod- tional difference between ceratopsians in DPP and MRM ied taxa like hadrosaurs and ceratopsians, are sensitive to is negligible. This stability between sampling areas is also relatively small environmental changes across the regional generally seen in the theropods (Fig. 6), with Troodon rep- palaeoenvironmental landscape [1–8, 11, 19–24, 27, 39, resenting the main exception, as it is not present in the 43, 70]. How this plays out over continental scales and earliest MRM site, appearing there later than in DPP. This between basins is currently unclear, but at least in terms was also noted by Brinkman et al. [14], and was attrib- of community composition measured at the family level, uted to southward migration/range-expansion. The later large bodied herbivore communities seem to exhibit little appearance of Troodon in MRM, along with an increase variation over the altitudinal transects considered here. in saurornitholestine material from the middle to upper Oldman Formation in MRM, may be a genuine change in Conclusions theropod assemblage that is not seen in DPP, or it may be The results of this study demonstrate that palaeoenvi- a result of sampling issues, as the middle Oldman Forma- ronmental setting is the primary driver of differences in tion of the MRM area is only represented by a single site vertebrate faunal assemblages throughout the Belly River (‘ORS’). The non-dinosaur component of the vertebrate Group, with palaeogeography/palaeolandscape acting as faunal assemblage was relatively stable across much of the another factor in structuring these assemblages. Depo- sampled interval, although there were considerable dif- sitional setting and stratigraphic interval do not have ferences in the relative abundances of taxa between DPP particularly strong effects on the preserved faunal assem- and MRM (Fig. 7), with batoids forming a much larger blage, confirming the results of other smaller-scale stud- component of the overall fauna in DPP. Unlike the pat- ies [14, 59]. tern shown in the broader vertebrate assemblages (Fig. 7), The subsample analyses of dinosaur and theropod there does not appear to be strong clustering according to assemblages, and their comparisons to the broader ver- sampling region in dinosaurs (Figs. 5a, 6a), suggesting that tebrate assemblages, suggest one of two possible conclu- the palaeogeographic signal in the broader analysis is due sions: either (a) dinosaur community composition is not to abundance differences (e.g. batoids) or rare/endemic sensitive to subtle changes in altitudinal and latitudinal taxa of non-dinosaurian affiliation (e.g. lissamphibians, palaeoenvironmental gradients, and/or (b) the differ- turtles, etc.). The similarity of faunal assemblages, and par- ences in environment between the pre-LCZ Dinosaur ticularly dinosaur assemblages, within the two terrestrial Park Formation of DPP and the upper Oldman Formation palaeoenvironmental settings (coastal plain vs. alluvial/ of MRM have been overstated. The higher proportion of inland) indicates that these subtle variations in terrestrial batoids in DPP than MRM across this same interval sug- palaeoenvironment may have less effect on faunal assem- gests that the more coastally-influenced terrestrial envi- blage structure than previously suggested [1, 12, 14], a ronment of DPP is genuine, refuting the long-held idea position supported by recent research on ceratopsids in that dinosaur communities were particularly sensitive the Oldman Formation of the Milk River/Manyberries to small-scale environmental gradients, such as paralic region [22]. It is also possible that the palaeoenvironmen- (coastal) to alluvial (inland) regimes within a single depo- tal interpretation of these formations and sampling areas sitional basin. Further research is required to fully answer

(See figure on next page.) Fig. 7 a R-mode vs. Q-mode cluster analysis of non-dinosaur component of Belly River Group microsites from the time-equivalent interval of the Oldman and Dinosaur Park formations of Dinosaur Provincial Park and Milk River/Manyberries. Dinosaur Provincial Park sites indicated with blue text and triangles. Milk River/Manyberries sites indicated with red text and circles. b Pair-wise Bray-Curtis similarity of Dinosaur Provincial Park (blue square) and Milk River/Manyberries (red square) microsite non-dinosaurian vertebrate relative abundance assemblages through lithostratigraphic record of time-equivalent Oldman and Dinosaur Park formations. c Formational average proportions of each non-dinosaurian vertebrate group in sampled regions. Taxonomic groups, site identifications, and other relevant information noted in legend Cullen and Evans BMC Ecol (2016) 16:52 Page 32 of 35

a

Adocus Chiloscyllium Chelydridae Mammalia Anura Squamata Esocidae Caudata + Allocaudata Teleostei indet. Coriops Champsosaurus ‘Holostean A’ Baenidae Tr ionychidae Phyllodontidae Eusuchia Lepisosteus Amiidae Acipenseriformes Belonostomus Myledaphus + Pseudomyledaphus ‘Holostean B’ Basilemys Paratarpon Hybodus CS (OM/upper ) HS (OM/upper ) PLS (OM/upper ) HAS (OM/upper ) RDS (OM/upper ) SalS (OM/upper ) CBC (OM/upper ) BMC (OM/upper ) CN−1 (OM/upper ) CN−2 (OM/upper ) BB71 (OM/Comrey) ORS (OM/Comrey) BB31 (DPF/pre-LCZ) BB98 (DPF/pre-LCZ) BB97 (DPF/pre-LCZ) BB86 (DPF/pre-LCZ) BB51 (DPF/pre-LCZ) BB78 (DPF/pre-LCZ) BB54 (DPF/pre-LCZ) BB25 (DPF/pre-LCZ) BB94 (DPF/pre-LCZ) BB75 (DPF/pre-LCZ) BB105 (OM/Comrey) BB103 (OM/Comrey) BB118 (OM/Comrey) BB107 (OM/Comrey) BB100 (OM/Comrey) BB121 (OM/Comrey) BB119 (DPF/pre-LCZ) BB108 (DPF/pre-LCZ) BB115 (DPF/pre-LCZ) BB104 (DPF/pre-LCZ) b BB120 (DPF/pre-LCZ) BB106 (DPF/pre-LCZ) BB117 (DPF/pre-LCZ) BB102 (DPF/pre-LCZ) Non-dinosaurs by Site: Pair-Wise Site Non-dinosaurs by Site: Similarity Dinosaur Provincial Park Through Lithostratigraphy Milk River / Manyberries

BB115 n i a BB119 l P l a BB108 t s a o

BB102 C r e

BB94 w o L /

BB75 c i l n i a r a l a

BB54 P P l a t

BB120 s a o C

BB106 r PLS e w o

BB25 (pre-LCZ ) HAS L / c i Dinosaur Park Fm . BB117 l BMC a r a

BB78 P SalS

BB104 CS

BB97 HS (upper unit ) Oldman Fm . n i a BB86 l RDS P l a BB51 t CN−1 s a o

BB31 C CN−2 r e p

BB98 p CBC U / l

BB107 a i n v i u a l l l

BB100 P A l a t

BB103 s a o C

BB121 r ORS e p p

BB71 Oldman Fm . U Oldman Fm . / l a BB118 i v u (middle unit / Comrey ss) l l (middle unit / Comrey ss )

BB105 A

0255075100 025 50 75 100 Percentage (%) 0 0.20.4 0.6 0.8 1.0 Percentage (%) c Bray-Curtis Similarity Taxa Averages by Lithostratigraphic Unit: Dinosaur Provincial Park LEGEND 100 Batoidea Caudata + Allocaudata 75

50 Selachimorpha Testudines 25 Chondrostei Squamata 0 Oldman Fm. (middle unit / Comrey ss) Oldman Fm. (upper unit) / Dinosaur Park Fm. (pre-LCZ) Holostei Choristodera Taxa Averages by Lithostratigraphic Unit: Milk River / Manyberries Teleostei Crocodylomorpha 100 Anura Mammalia 75

50 Dinosaur Provincial Park Sites Milk River / Manyberries Sites 25 0 Dinosaur Provincial Park Milk River / Manyberries Oldman Fm. (middle unit / Comrey ss) Oldman Fm. (upper unit) / Pairwise Similarity Curve Pairwise Similarity Curve Dinosaur Park Fm. (pre-LCZ) Cullen and Evans BMC Ecol (2016) 16:52 Page 33 of 35

this question, but it is possible that consistently high rates References 1. Gates TA, Sampson SD, Zanno LE, Roberts EM, Eaton JG, Nydam RL, of evolution and niche partitioning among species within Hutchison JH, Smith JA, Loewen MA, Getty MA. Biogeography of ter- each of the sampled dinosaur families played a greater restrial and freshwater vertebrates from the late Cretaceous (Campanian) role in the observed high diversity and frequent turno- Western Interior of North America. Palaeogeogr Palaeoclimatol Palaeo- ecol. 2010;291(3–4):371–87. vers in dinosaur taxa throughout the Late Cretaceous of 2. Lehman TM. Late Cretaceous dinosaur provinciality. In: Tanke D, Carpenter North America. K, editors. Mesozoic vertebrate life. Ottawa: NRC Research Press; 2001. p. 310–28. Additional files 3. Sampson SD, Loewen MA, Farke AA, Roberts EM, Forster CA, Smith JA, Titus AL. New horned dinosaurs from Utah provide evidence for intracon- tinental dinosaur endemism. PLoS ONE. 2010;5(9):e12292. 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Sea level, This study did not involve research on human subjects. dinosaur diversity and sampling biases: investigating the ‘common cause’ hypothesis in the terrestrial realm. Proc R Soc Lond B Biol Sci. Ethics 2011;278(1709):1165–70. This study did not involve regulated animal species. All specimens analyzed in 18. Dunhill AM, Bestwick J, Narey H, Sciberras J. Dinosaur biogeographical this project represent the fossilized remains of ancient/extinct species. structure and Mesozoic continental fragmentation: a network-based approach. J Biogeogr. 2016;43:1691–704. doi:10.1111/jbi.12766. Funding 19. Horner J. The Mesozoic terrestrial ecosystem of Montana. In: Montana Funding provided to T.M.C through a Natural Sciences and Engineering Geological Society Field Conference; 1989. Research Council Alexander Graham Bell Canada Graduate Scholarship 20. Horner J. Three ecologically distinct vertebrate faunal communities from (CGSD3-444747-2013), and to D.C.E through a Natural Sciences and Engineer- the Late Cretaceous two medicine formation of Montana, with discussion ing Research Council Discovery Grant (RGPIN 355845). of evolutionary pressures induced by interior seaway fluctuations. In: Montana Geological Society Field Conference; 1984. Received: 3 June 2016 Accepted: 29 October 2016 21. Bell PR, Currie PJ. A high-latitude dromaeosaurid, Boreonykus certekorum, gen. et sp. nov. (Theropoda), from the upper Campanian Wapiti Forma- tion, west-central Alberta. J Vertebr Paleontol. 2016;36(1):e1034359. Cullen and Evans BMC Ecol (2016) 16:52 Page 34 of 35

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