Pure Spatial and Spatially Structured Environmental Variables Explain Skistodiaptomus Copepod Range Limits in the Northeastern USA

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Pure spatial and spatially structured environmental variables explain Skistodiaptomus copepod range limits in the northeastern USA

Ryan A. Thum and Richard S. Stemberger

Abstract: We assessed the ability of present-day environmental factors to explain the nonoverlapping range boundaries of Skistodiaptomus copepods in the northeastern USA. Variance partitioning using partial canonical correspondence analysis (CCA) attributed 21% of the variance in species occurrences to spatial location, 20% to spatially structured environmental variation, and 12% to environmental factors that are not spatially structured. Discriminant function analysis (DFA) aided our interpretation of the variance in species’ occurrences attributed to spatially structured environmental variation. Skistodiaptomus pallidus lakes were discriminated from Skistodiaptomus oregonensis and Skistodiaptomus pygmaeus lakes along a productivity gradient, with S. pallidus occurring in more productive lakes. In contrast, S. oregonensis and S. pygmaeus lakes were environmentally similar. Thus, a large portion of the spatially structured variation in the variance-partitioning analysis most likely reflected the shared correlations between the spatial locations and environmental conditions of S. pallidus lakes. Taken together, the results from CCA and DFA analyses suggested that S. pallidus’ range boundary is controlled by environmental factors (lake productivity), while the range boundaries for S. oregonensis and S. pygmaeus were related more to their biogeographic histories than to present-day environments. We discuss alternative explanations for range limits that are independent of environmental conditions. Résumé : Nous avons évalué dans quelle mesure les facteurs environnementaux d’aujourd’hui permettent d’expliquer les répartitions des aires géographiques discrètes des copépodes Skistodiaptomus dans le nord-est des É.-U. Une partition de la variance par analyse des correspondantes canoniques (CCA) partielles attribue 21 % de la variance dans la présence des espèces à la position géographique, 20%àdelavariationenvironnementale à structure spatiale et 12 % à des facteurs environnementaux qui ne sont pas structurés en fonction de l’espace. Une analyse des fonctions discrimi- nantes (DFA) a contribué à l’interprétation de la variance dans la présence des espèces attribuée à la variation environ- nementale reliée à l’espace. Les lacs à Skistodiaptomus pallidus se distinguent des lacs à Skistodiaptomus oregonensis et à Skistodiaptomus pygmaeus d’après un gradient de productivité, S. pallidus se retrouvant dans les lacs plus produc- tifs. En revanche, les lacs à S. oregonensis et à S. pygmaeus possèdent des environnements semblables. Ainsi, une portion importante de la variation à structure spatiale dans l’analyse de partition de la variance reflète très vraisemblablement les corrélations communes entre les positions géographiques et les conditions environnementales des lacs à S. pallidus. Pris dans leur ensemble, les résultats des analyses CCA et DFA indiquent que les limites de l’aire de répartition de S. pallidus sont contrôlées par des facteurs environnementaux (productivité des lacs), alors que les limites d’aire de S. oregonensis et de S. pygmaeus sont reliées plus à leur histoire biogéographique qu’à leur environ- nement d’aujourd’hui. Des explications de rechange des limites d’aire qui sont indépendantes des conditions environnementales font l’objet d’une discussion. [Traduit par la Rédaction] Thum and Stemberger 1404

Introduction range limits may be set by physiological constraints to abiotic conditions (e.g., Root 1988), habitat selection (e.g., Species’ ranges may reflect both contemporary ecological States 1976; Howard and Harrison 1984; Alkon and Saltz interactions and historical contingencies (Endler 1982a, 1988), or the presence of natural enemies that exclude them. 1982b). When dispersal opportunities are not limiting, spe- However, geographic ranges may also be limited by factors cies’ ranges should reflect present-day variation in environ- that are not necessarily related to environmental conditions. mental conditions that define geographic boundaries between For example, limitations to dispersal (e.g., dependence on local habitats that do or do not support positive population continuous water routes) can influence species’ range limits growth (e.g., Caughley et al. 1987; Root 1988). For example, if dispersal opportunities are available in some but not all di-

Received 6 July 2005. Accepted 22 December 2005. Published on the NRC Research Press Web site at http://cjfas.nrc.ca on 13 May 2006. J18776 R.A. Thum1,2 and R.S. Stemberger. Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA. 1Corresponding author (e-mail: [email protected]). 2Present address: Department of Ecology and Evolutionary Biology, E303 Corson Hall, Cornell University, Ithaca, NY 14853, USA.

Can. J. Fish. Aquat. Sci. 63: 1397–1404 (2006) doi:10.1139/F06-046 © 2006 NRC Canada 1398 Can. J. Fish. Aquat. Sci. Vol. 63, 2006 rections (Gaylord and Gaines 2000). Similarly, populations mental variance, (b) spatially structured environmental vari- may experience Allee effects that prevent range expansion ance, and (c) pure spatial variance that is independent of beyond their current limits (Keitt et al. 2001). Finally, range environmental variance (Borcard et al. 1992). If species’ dis- limits may be defined by biological interactions (e.g., inter- tributions correspond to variation in environmental factors, ference competition, reproductive interference, hybridization) then the explained variance in species’ occurrences should with adjacently distributed (parapatric) species, and these in- be attributed to either pure or spatially structured environ- teractions need not be mediated by the environment (Bull mental variation. On the other hand, when species’ distribu- 1991; Case et al. 2005). tions are limited by factors other than environmental Biogeographic analyses of zooplankton distributions in ar- conditions, we expect spatial location independent of envi- eas of North America that were glaciated during the Pleisto- ronmental variation to largely explain species’ occurrences. cene have revealed strong associations between the current Thus, the relative importance of spatial and environmental distributions of many species and historical waterway con- variables can be used to infer the relative influence of connections (e.g., proglacial lakes) to presumed areas of glacial temporary environment in determining species’ range limits. refugia (Dadswell 1974; Carter et al. 1980; Stemberger Here we take advantage of a large data set of environmen- 1995). While these associations suggest that dispersal limita- tal conditions for lakes across the range boundaries of north- tion across wide biogeographic spatial scales contributes eastern USA Skistodiaptomus to evaluate the relative substantially to species’ geographic range limits, they do not influences of contemporary environmental differences versus preclude an important role of contemporary environmental factors unrelated to the environment in maintaining their dis- conditions for maintaining range limits. For example, strong tribution boundaries. We use partial canonical correspon- correlations may exist between the geological history of an dence analysis (CCA; ter Braak 1986; Borcard et al. 1992; area and present-day environmental conditions. Moreover, ter Braak and Šmilauer 2002) to determine the relative influ- zooplankton are thought to disperse effectively because of ences of environmental variables and spatial locations to ex- the prevalent production of resting stages that can presum- plain Skistodiaptomus occurrences. We then use discriminant ably disperse readily through animal vectors (Maguire 1963; function analysis (DFA) to determine whether lakes occu- Proctor 1964). In addition, recent experimental evidence pied by different species are discriminated by local environ- suggests that local processes are more important than dis- mental conditions. Although similar to the CCA in its persal limitation in determining local zooplankton composi- methodology, DFA is used to explicitly test the hypothesis tion across small spatial scales (Shurin 2000). However, the that Skistodiaptomus species occupy lakes that are signifi- influence of dispersal versus environmental limitations on cantly different in their environmental conditions. The DFA zooplankton distributions may vary across taxa (Jenkins and allows multiple comparisons between species, which in turn Buikema 1998; Jenkins and Underwood 1998; Bohonak and facilitates the interpretation of the spatially structured Jenkins 2003). Thus, biogeographic studies should explicitly environmental component (b) in the CCA. For example, test for an influence of contemporary environmental condi- discriminant functions that significantly distinguish Skisto- tions and factors that are independent of the environment in diaptomus oregonensis lakes from Skistodiaptomus pygmaeus determining species’ ranges. lakes indicate longitudinal gradients in environmental vari- Copepods in the genus Skistodiaptomus that occur in the ables contributing heavily to that function, since these spe- northeastern United States and adjacent Canada provide a cies are spatially segregated across the landscape along a unique opportunity to study the relative importance of present- longitudinal axis (see Fig. 1). day environmental factors versus other factors for determin- Using CCA and DFA in conjunction, we show that spa- ing species’ range limits. Associations between current dis- tially structured environmental variation largely explains tributions and historical waterways suggest historical Skistodiaptomus pallidus occurrences, while spatial location dispersal limitation to the large proglacial lakes that formed independent of environmental variation explains the majority along the retreating edge of the Wisconsinan glacier, and of variation in S. oregonensis and S. pygmaeus occurrences. these lakes ultimately connected to the isolated glacial refugia from which they likely colonized (Stemberger 1995; Fig. 1). Materials and methods Moreover, these species do not appear to be as effective dispersers as other zooplankton groups (Stemberger 1995), Skistodiaptomus and environmental data were obtained from and thus their distributions may be limited by factors that are the US Environmental Protection Agency Environmental Mon- not necessarily related to present-day environmental condi- itoring and Assessment Program – Surface Waters survey of tions. However, differences in contemporary environmental northeastern USA lakes (available from http://www.epa.gov/ conditions among lakes occupied by these species have not emap/html/dataI/surfwatr/data/nelakes/index.html). This data been explicitly evaluated as a factor maintaining Skisto- set consists of 614 sampling dates for 373 lakes in New diaptomus distributions. England, New Jersey, and New York during the months of A variety of statistical techniques have been developed to July–August 1991–1996. Of these lakes, 253 were sampled relate variance in species’ occurrences to variance in envi- once and 120 were sampled more than once (up to seven ronmental conditions (e.g., Legendre and Legendre 1998; ter times). Six lakes were excluded because they lacked zoo- Braak and Šmilauer 2002). In addition, the inclusion of spa- plankton data. tial locations (i.e., geographic location of lakes in the study We selected a single sampling date from each of the lakes area) as explanatory variables can be used to decompose the that were sampled more than once over the period of 1991– explained variance in species’ occurrences into three frac- 1996 to satisfy assumptions of statistical independence. We tions that correspond to (a) spatially independent environ- randomly selected a sampling date from each lake where a

Fig. 1. Distributions of Skistodiaptomus species in the northeastern USA based on species occurrence from the Environmental Monitoring and Assessment Program data (available from http://www.epa.gov/emap/html/dataI/surfwatr/data/nelakes/index.html). Skistodiaptomus species show little overlap in their distributions except in southern New England. Shaded circles, Skistodiaptomus oregonensis; solid triangles, Skistodiaptomus pygmaeus; open squares, Skistodiaptomus pallidus.

Skistodiaptomus was either present or absent on all visits larly, we square-root-transformed species richness variables. (354 lakes). If a Skistodiaptomus was present in some but pH was not transformed, as it was already measured on a log not all sampling visits, we randomly chose a sampling date scale. Because of negative values, ANC was transformed by from which the species was present (13 lakes) to maximize taking the log10 of the absolute value of each measurement our power to discriminate among lakes inhabited by differ- and then adjusting the sign depending on the sign of the ent species. Skistodiaptomus may have been present in some original measurement. lakes without detection if the adult stages upon which species identifications are based were not observed. However, Influence of environmental versus spatial factors on failure to detect Skistodiaptomus in some lakes did not bias Skistodiaptomus occurrences our analyses because we only made statistical comparisons We performed partial CCA (ter Braak 1986) using among lakes where Skistodiaptomus were present; we did CANOCO, version 4.5 (ter Braak and Šmilauer 2002) for not attempt to compare lakes with and without particular variance partitioning described by Borcard et al. (1992). CCA Skistodiaptomus. Sample sizes of lakes containing is the preferred method for relating explanatory variables to S. pallidus, S. oregonensis, and S. pygmaeus were 24, 34, presence or absence data (Legendre and Legendre 1998). and 72, respectively. Briefly, three separate CCAs were performed: one using en- In all analyses, we related presence or absence data for vironmental variables, one using spatial variables, and one Skistodiaptomus to a number of physicochemical, nutrient, using both environmental and spatial variables. Because of hydrological, and biological variables (see Table 1). We used the potential for shared portions of variance due to correla- conductivity, pH, and acid-neutralizing capacity (ANC) as tions between environmental variables and spatial location, surrogates for all ion concentrations because they are highly the environmental CCA explains a fraction of variance (a + correlated (r > |0.8|). We log10-transformed continuous vari- b) that includes a spatially structured component (b). Simi- ables such as chemical variables and species abundances to larly, the spatial CCA explains a fraction of variance (b + c) satisfy assumptions of normality and equal variance. Simi- that includes this same spatially structured environmental

Table 1. Means and ranges of environmental variables used in canonical correspondence and discriminant function analyses for three Skistodiaptomus species. S. oregonensis S. pygmaeus S. pallidus Variable Mean Min.–Max. Mean Min.–Max. Mean Min.–Max. Hydrological Lake area (ha) 201.9 1.6–1229.7 205.2 1.5–4284.5 49.5 1.8–730.9 Average depth (m) 4.7 0.6–19.4 4.1 0.6–21.9 2.9 0.6–18.5 Retention (years) 0.5 0–4.1 0.5 0–3.4 0.2 0–2.3 Elevation (m) 365.8 22.0–600.0 176.5 2–555.0 218.4 11.0–568.0 Physicochemical pH 7.3 4.5–8.7 7.2 4.2–8.5 8.2 7.5–8.6 ANC (µequiv.·L–1) 484.1 –2621.5 208.5 –1612.2 1099.1 188.0–2963.0 Conductivity (µS·cm–1) 92 10.4–692.2 86.2 17.6–688.0 223 76.6–660.0 Color (PCU) 28.6 3.0–193.0 27.8 2.0–299.0 24.3 3.0–126.0 Turbidity (NTU) 1 0.3–3.2 1.1 0.3–6.7 6.2 0.6–31.0 Total suspended solids (mg·L–1) 1.9 0.3–4.8 1.6 0–7.8 11.9 0.6–116.0 Nutrients TotalP(µg·L–1) 15.3 3.6–62.0 12.7 0–55.0 441.3 6.0–8740.0 TotalN(µg·L–1) 406.9 202.0–1018.0 382.6 148.0–2524.0 1088.9 300.0–4013.0 N/P 3.5 2.0–4.4 3.4 0–6.6 2.7 0–4.1 Biological Chlorophyll a (µg·L–1) 7.9 1.2–43.5 4.9 0–28.5 42 1.8–191.9 Species richness (no. of species) Small cladocerans 3.2 0–7.0 3.7 1.0–9.0 4.2 1.0–10.0 Large cladocerans 3.1 0–6.0 3.1 0.0–10.0 2 1.0–7.0 Small cyclopoids 0.4 0–1.0 0.6 0.0–1.0 0.6 0–1.0 Large cyclopoids 1.7 0–5.0 1.5 0–4.0 1.3 0–5.0 Calanoid copepods 1.8 0–3.0 1.9 1–5.0 1.3 0–5.0 Crustaceans 10.2 0–16.0 10.6 1.0–24.0 9.1 0–21.0 Rotifers 20.2 0–35.0 18.4 0–37.0 18.6 0–38.0 Species abundance (individuals·L–1) Small cladocerans 7.3 0–59.9 6.5 0–123.3 39.8 0.2–267.1 Large cladocerans 5.8 0–27.1 9.3 0–263.5 15.9 0–138.3 Large adult cyclopoids 3.4 0–22.8 4 0–28.3 14.3 0–154.2 Adult Epischura 0.1 0–1.3 0.1 0–1.0 0.1 0–7.8 Rotifers 292.6 0–2273.2 244.7 0.3–1701.4 1041.2 18.4–5466.7 Note: Not all variables entered into the analyses significantly (α = 0.05; see text for details). ANC, acid-neutralizing capacity; PCU, platinum–cobalt units; NTU, nephelometric turbidity units. component. The CCA incorporating both spatial and envi- 0.05. Spatial variables consisted of decimal degrees longi- ronmental variables explains the total variation in species tude and latitude coordinates of lake locations. Variables occurrences (a + b + c). Thus, the spatially structured envi- were included if they explained a significant amount of ad- ronmental component of variance (b) can be determined from ditional variance at α = 0.05. In addition, we inspected vari- the equation: ance inflation factors (VIFs) and eliminated variables with VIFs > 20 (ter Braak and Šmilauer 2002). babbcabc=[( +++ ) ( )] −++ ( )

The pure environmental (a) and pure spatial (c) components Environmental differences among Skistodiaptomus lakes can then be determined by subtraction: We used DFA to determine if lakes occupied by different aabb=+−() Skistodiaptomus species could be distinguished from one another based on their environmental conditions using and STATISTICA, version 7.1 (StatSoft Software, Inc., Tulsa, Oklahoma). cbcb=+−() As in the CCA, we chose the environmental variables to We used the forward selection procedure in CANOCO and include in the DFA by using the forward selection procedure 1000 Monte Carlo permutation tests for selecting environ- with α = 0.05. In addition, we only allowed variables with mental (see Table 1) and spatial variables to include in the tolerances >0.1 to enter. Tolerance ranged from 0 to 1 and is partial CCAs (ter Braak and Šmilauer 2002) with an α = a measure of the unique contribution of an environmental

Table 2. Variance partitioning and associated P val- Table 3. Comparison of marginal and conditional λ values for ues for canonical correspondence analyses with spa- canonical correspondence analyses. tial and environmental variables based on 1000 λ Monte Carlo permutations. Conditional Variable Marginal λ abc Partition Variance explained (%) P Longitude 0.57 — 0.57 0.57 a + b + c 53.0 0.001 Latitude 0.23 — 0.12 0.24 a + b 32.2 0.001 Turbidity 0.41 0.41 0.30 — a + c 40.6 0.001 Total N 0.36 0.09 0.03 — a 12.4 Elevation 0.12 0.08 0 — b 19.6 pH 0.18 0.06 0.04 — c 21.0 Note: Marginal λ refers to the variance in species occurrences ex- Unexplained 47.0 plained by the variable alone. Conditional λ refers to the additional vari- Note: Values represent the percentage of variation in ance in species occurrences explained after the inclusion of other variables Skistodiaptomus occurrences explained by the first two ca- in the forward selection procedure. Variance components: pure environ- nonical axes. Pure environmental (a), spatially structured mental (a), spatially structured (b), and pure spatial (c). (b), and pure spatial (c) variance components and their combinations are shown. Both canonical axes were significant at α = 0.001. Table 4. Factor structures of the two discriminant functions (DF) for Skistodiaptomus lakes. Variable DF1 DF2 Tolerance* variable to the overall analysis — higher numbers reflect greater unique contribution to the analysis. We applied pH 0.39 –0.09 0.82 Levene’s tests on all environmental variables to check for Color –0.04 0.06 0.56 heterogeneity of variances among groups. Turbidity 0.70 –0.46 0.51 Predation by fish is a major factor structuring body size Total N 0.67 –0.06 0.37 and species composition of zooplankton assemblages (Currie Lake area –0.29 –0.06 0.64 et al. 1999). We did not include any fish variables in our Average lake depth –0.22 0.22 0.50 multivariate analyses because of missing data for many lakes Elevation 0.00 0.81 0.89 (only 11 and 18 lakes with S. oregonensis and S. pallidus *Tolerance is a measure of the redundancy of explanatory variables. present, respectively, had fish data). To maintain the higher sample sizes for multivariate analyses, we analyzed the total counts of fish (which included young-of-the-year fish, juve- mental variation explained the least amount of variance in niles, and adults) for all Skistodiaptomus lakes for which species occurrences (23%). Moreover, the relative impor- these data were available using univariate analysis of vari- tance of environmental variables in explaining species oc- ance (ANOVA). These data were log10-transformed before currences decreased when spatial variables were also analysis to satisfy the assumption of homogeneity of vari- included (Table 3). For example, elevation failed to explain ances among groups. Collection effort was dependent on any additional variance in species occurrences when spatial lake size and is described in Baker et al. (1997). location was also considered (Table 3).

Results Environmental differences among Skistodiaptomus lakes Seven environmental variables entered significantly into Influence of environmental versus spatial factors on the DFA: pH, color, turbidity, total nitrogen, average lake Skistodiaptomus occurrences depth, and elevation. Turbidity, total nitrogen, and pH con- Forward selection identified four environmental variables tributed most heavily to discriminant function one (DF1), that entered significantly into the CCA: turbidity, total nitro- while elevation, turbidity, and average lake depth contributed gen, elevation, and pH. ANC was significant using forward most heavily to DF2 (Table 4). selection but had a high VIF because of its high correlation The DFA produced two canonical axes (discriminant func- with pH. Therefore, we included pH and eliminated ANC. tions) that were significant at α = 0.01. The overall DFA had All other environmental variables (see Table 1) failed to en- a Wilks’ λ (a measure of discriminatory power, where 0 is ter significantly into the analysis using forward selection cri- perfect discrimination and 1 is no discriminatory power) of teria. Both longitude and latitude entered significantly into 0.38. However, the second discriminant function had poor the model using a forward procedure with only spatial vari- discriminatory power (Wilks’ λ = 0.84). This poorer dis- ables. criminatory power of the second discriminant function is be- Spatial and environmental variables together explained 53% cause DFA partitions variance among groups such that the of the variation in Skistodiaptomus occurrences (Table 2). most variance is explained by the first axis, followed by the The majority (40%) of this variation was attributed to spatial second axis, and so on. location independent of the environment. In fact, forward se- Multiple comparisons of species indicated that the envi- lection revealed that longitude alone was the greatest single ronments of lakes occupied by different Skistodiaptomus were predictor of species occurrences (Table 3). However, a pure significantly different at α = 0.001. A scatterplot of DF1 spatially structured environmental component also contrib- scores versus DF2 scores demonstrates that DF1 discrimi- uted heavily to the explained variance (37%). Pure environ- nates S. pallidus from S. oregonensis and S. pygmaeus, while

Fig. 2. Scatterplot of scores from overall discriminant functions Fig. 3. Mean and standard errors for total fish counts for lakes among lakes occupied by different Skistodiaptomus species. occupied by different Skistodiaptomus species. Letters above bars There is clear separation of Skistodiaptomus pallidus from indicate multiple comparisons, where identical letters indicate Skistodiaptomus oregonensis and Skistodiaptomus pygmaeus groups that are not significantly different (α = 0.05). along discriminant function 1, which is driven largely by variables related to productivity. Discriminant function 2 is largely driven by elevation, which separates S. oregonensis and S. pygmaeus. Shaded circles, S. oregonensis; solid triangles, S. pygmaeus; open squares, S. pallidus.

tion a), spatially structured environmental variation (fraction b) also explains a sizeable fraction of Skistodiaptomus occurrences. The pure spatial component of variance is consistent with Stemberger’s (1995) suggestion that dispersal limitation to historical waterway connections to isolated glacial refugia explains the nonoverlapping ranges of Skisto- diaptomus in the northeastern USA. However, the spatially structured environmental component of variance suggests that landscape-level environmental gradients may also maintain these nonoverlapping boundaries. DF2 discriminates S. oregonensis from S. pallidus and DFA further revealed the relative contributions of spatial S. pygmaeus (Fig. 2). Although significantly different, ex- versus environmental factors accounting for Skistodiaptomus amination of the classification of cases based on the discri- occurrences in northeastern lakes. In particular, it suggests minant functions revealed that S. oregonensis lakes were that the northern range limit of S. pallidus in the northeast- commonly misclassified as S. pygmaeus lakes (47% of ern USA is determined by environmental factors, while the S. oregonensis lakes misclassified as S. pygmaeus lakes). eastern and western range limits of S. oregonensis and Skistodiaptomus pallidus and S. pygmaeus lakes were cor- S. pygmaeus, respectively, are determined by spatial location rectly classified as such in 75% and 90% of the cases, re- independent of environmental variables. spectively. Lakes occupied by S. pallidus were clearly different in Finally, one-way ANOVAs performed on the total fish their environmental characteristics from those occupied by counts further supported strong environmental differentia- S. oregonensis or S. pygmaeus. In short, S. pallidus lakes tion of lakes occupied by S. pallidus. Total fish counts sig- were more productive than S. oregonensis or S. pygmaeus nificantly differed among lakes occupied by different lakes: they were more turbid and had higher total nitrogen and pH. In addition, S. pallidus lakes also had higher num- Skistodiaptomus (F[2,58] = 5.2, p = 0.008); Newman–Keuls multiple comparisons showed that S. pallidus lakes had sig- bers of fish and smaller-bodied zooplankton assemblages dominated by high abundances of small cladocerans, early nificantly more fish (mean of log10-transformed data = 2.8, n = 18) than lakes having either S. pygmaeus (mean of instars of cyclopoid copepods, and rotifers although these variables were either not included (i.e., fish data) or did not log10-transformed data = 1.2, n = 33) or S. oregonensis (mean enter significantly into the overall DFA or CCA. Dominance of log10-transformed data = 1.5, n = 11). However, total fish counts between S. oregonensis lakes and S. pygmaeus lakes by small-bodied species most likely reflected the intensity of did not significantly differ (Fig. 3). size-selective predation by fish (Stemberger and Miller 2003). However, lake productivity was also positively corre- Discussion lated with higher numerical abundances of small cladocerans, cyclopoid copepods, and rotifers (Stemberger and Lazorchak The variance-partitioning CCA demonstrates that spatial 1994). Thus, S. pallidus occupation of more productive lakes location explains the vast majority of the variation in Skisto- may reflect either its physiological tolerance to abiotic con- diaptomus occurrences in the northeastern USA. Although ditions, its ability to prey on small zooplankton-like rotifers the largest component of variance is attributed to pure spa- (Williamson and Butler 1987), or its ability to reduce im- tial variance independent of environmental variation (frac- pacts on its population growth rate by effectively avoiding

© 2006 NRC Canada Thum and Stemberger 1403 fish predators. Regardless of the biological mechanism, that Allee effects may play an important role in determining S. pallidus’ northern boundary in the northeastern USA ap- occurrences for copepods. For example, weak overland dis- pears to be environmentally controlled by variables associ- persal ability and Allee effects appear to limit the ability of ated with higher productivity. the diaptomid copepod Hesperodiaptomus shoshone to rees- The environmental differences between S. pallidus lakes tablish populations in ponds where it occurred before the in- versus S. oregonensis and S. pygmaeus lakes are consistent troduction of fish populations, even after fish removal with previous descriptions of S. pallidus. For example, cul- (Sarnelle and Knapp 2004). However, zooplankton are gen- tural eutrophication of lakes has been recognized as a factor erally thought to disperse effectively because of their pro- promoting S. pallidus’ range expansion in the western USA duction of resting stages that can be easily transported by (Byron and Saunders 1981) and Wisconsin (Torke 2001) animal vectors, such as birds (Maguire 1963; Proctor 1964; from areas in which it historically occurred. Recent land use Figuerola et al. 2005). Thus, dispersal limitation is not ex- changes due to increased agricultural development in the pected to be a major factor involved in limiting species’ dis- southern region of our study area have occurred to a greater tributions (e.g., Shurin 2000). An alternative explanation is extent than in the northern region and may therefore explain that direct interactions between S. oregonensis and why S. pallidus is the most dominant Skistodiaptomus in this S. pygmaeus prevent their range overlap despite their dis- region. persal abilities. Although models for competitive parapatry In contrast with S. pallidus, lakes occupied by S. ore- over homogeneous space are rare (Bull 1991), one mecha- gonensis and S. pygmaeus were similar in the majority of en- nism is reproductive interference (decreases in the reproduc- vironmental variables, with the exception of lake elevation: tive fitness of females due to physical blocking or damaging S. oregonensis tended to occur in higher-elevation lakes. of genitalia by indiscriminant mating with heterospecific However, lake elevation itself is spatially structured across males; Bull 1991; Case et al. 2005). Skistodiaptomus orego- the landscape: lakes in the western portions of our study area nensis and S. pygmaeus males will mate readily with hetero- (where S. oregonensis occurs) are generally higher than in specific females despite zero production of offspring eastern portions (where S. pygmaeus occurs). In a separate (S. oregonensis males crossed with female S. pygmaeus)or DFA (not shown), we included longitude as an independent the production of intrinsically incompatible offspring that variable. The inclusion of longitude in the forward selection die before their first molt (S. pygmaeus males crossed with procedure resulted in the elimination of elevation as a signif- S. oregonensis females; Thum 2004). Moreover, a recently icant variable in the model (p = 0.55). This indicates that the completed experiment demonstrates that the presence of strong influence of lake elevation on the discrimination of heterospecific males decreases the probability of successful S. oregonensis and S. pygmaeus lakes results from the corre- fertilization of both S. oregonensis and S. pygmaeus females lation between lake location and elevation. Another DFA (R. Thum, unpublished data). Thus, there is a strong oppor- (not shown) where neither elevation of longitude was in- tunity for reproductive interference, which has been demon- cluded resulted in insignificant differences between S. ore- strated to maintain stable parapatry (Anderson 1977; Bull gonensis and S. pygmaeus lakes (p = 0.25). 1991; Case et al. 2005). The slight difference in mean lake elevations between It is possible that our analysis failed to incorporate some S. oregonensis and S. pygmaeus probably has little biological spatially structured environmental variables that influence relevance and more likely reflects the influence of dispersal Skistodiaptomus occurrences (Legendre and Legendre 1998), from geographically isolated glacial refugia, as suggested by and 37% of the variance in species occurrences remains un- Stemberger (1995). The higher elevations of lakes currently explained. This explanation is unlikely because important occupied by S. oregonensis, particularly in the Adirondack environmental variables that we failed to incorporate would province, are at much higher elevation today than they were have to be uncorrelated with all of the variables that we in- at the onset of glacial retreat because of extensive isostatic cluded, and this list is comprehensive. rebound of the underlying bedrock since deglaciation. Al- Separating the influence of history and contemporary though lake elevation can influence environmental condi- environmental factors that explain occurrences of these spe- tions such as water chemistry (e.g., Webster et al. 1996; cies will likely require a variety of investigations that ad- Webster et al. 2000), elevation differences between S. ore- dress alternative hypotheses, as suggested by Endler (1982b). gonensis and S. pygmaeus lakes are not accompanied by en- Our analyses make important headway on untangling the rel- vironmental differences in other variables. ative influences of contemporary environmental factors and The environmental similarities among lakes occupied by historical contingencies in determining species’ ranges. Spe- S. oregonensis and S. pygmaeus suggest that factors other cifically, we extend our understanding of the drivers of range than contemporary environments may have played an impor- limits for zooplankton following colonization from Pleisto- tant role in maintaining their historic range limits following cene refugia. Previous interpretations of zooplankton distri- their initial colonization of the northeastern USA at the end butions in the northeastern USA and Canada were based of the Pleistocene. As Stemberger (1995) suggested, dis- almost solely on spatial occurrence data (e.g., Dadswell persal limitation to water vector transport may have pre- 1974; Carter et al. 1980; Stemberger 1995); we have explic- served the historical range limits of these two species itly incorporated environmental and spatial factors into a sin- following colonization of interior North America from iso- gle analysis. Our results suggest that environmental factors lated glacial refugia using the extensive proglacial lake and related to lake productivity may limit the spread of some drainage connections. This interpretation implicitly invokes zooplankton species that expanded from their Pleistocene Allee effects that prevent range expansion beyond current refugia following glacial retreat. However, environmental limits (e.g., Keitt et al. 2001), and there is some evidence similarities among lakes occupied by different species of

© 2006 NRC Canada 1404 Can. J. Fish. Aquat. Sci. Vol. 63, 2006 these copepods suggest that factors other than environmental Howard, D.J., and Harrison, R.G. 1984. Habitat segregation in differences have prevented the spread of some species from ground crickets: the role of interspecific competition and habitat the areas they originally colonized via extensive waterway selection. Ecology, 65: 69–76. connections following ice sheet retreat. Further investigation Jenkins, D.G., and Buikema, A.L., Jr. 1998. Do similar communi- of alternative hypotheses for range limits that do not depend ties develop in similar sites? A test with zooplankton structure on environmental conditions should broaden our understand- and function. Ecol. Monogr. 68: 421–443. ing of the interactions between species’ ecologies and their Jenkins, D.G., and Underwood, M.O. 1998. Zooplankton may not dis- histories in determining geographic ranges. perse readily in wind, rain, or waterfowl. Hydrobiologia, 387/388: 15–21. Keitt, T.H., Lewis, M.A., and Holt, R.D. 2001. Allee effects, inva- Acknowledgements sion pinning, and species’ borders. Am. Nat. 157: 203–216. We thank K.L. Cottingham, J.J. Gilbert, R.G. Harrison, M.A. Legendre, P., and Legendre, L. 1998. Numerical ecology. 2nd ed. McPeek, J. Jones, K. Peterson, B. Brown, N.G. Hairston, Jr., T. Elsevier, Amsterdam. Yoshida, C. Kearns, and J. Fox for helpful comments. Maguire, B.J. 1963. The passive dispersal of small aquatic organ- isms and their colonization of isolated bodies of water. Ecol. Monogr. 33: 161–185. References Proctor, V.W. 1964. Viability of crustacean eggs recovered from Alkon, P.U., and Saltz, D. 1988. Foraging time and the northern ducks. Ecology, 45: 656–658. range limits of the Indian crested porcupine (Hystrix indica Kerr). Root, T. 1988. Energy constraints on avian distributions and abun- J. Biogeogr. 15: 403–408. dances. Ecology, 69: 330–339. Anderson, R.F.V. 1977. Ethological isolation and competition of Sarnelle, O., and Knapp, R.A. 2004. Zooplankton recovery after allospecies in secondary contact. Am. Nat. 111: 939–949. fish removal: limitations of the egg bank. Limnol. Oceanogr. 49: Baker, J., Peck, D., and Sutton, D. 1997. Environmental monitoring 1382–1392. and assessment program surface waters: field operations manual Shurin, J.B. 2000. Dispersal limitation, invasion resistance, and the for lakes. US Environmental Protection Agency, Washington, D.C. structure of pond zooplankton communities. Ecology, 81: 3074– Bohonak, A.J., and Jenkins, D.G. 2003. Ecological and evolution- 3086. ary significance of dispersal by freshwater invertebrates. Ecol. States, J.B. 1976. Local adaptations in chipmunk Eutamias amoenus Lett. 6: 783–796. populations and evolutionary potential at species borders. Ecol. Borcard, D., Legendre, P., and Drapeau, P. 1992. Partialling out the Monogr. 46: 221–256. spatial component of ecological variation. Ecology, 73: 1045– Stemberger, R.S. 1995. Pleistocene refuge areas and postglacial 1055. dispersal of copepods of the northeastern United States. Can. J. Bull, C.M. 1991. Ecology of parapatric distributions. Annu. Rev. Fish. Aquat. Sci. 52: 2197–2210. Ecol. Syst. 22: 19–38. Stemberger, R.S., and Lazorchak, J.M. 1994. Zooplankton assem- Byron, E.R., and Saunders, J.F. 1981. Colonization of Lake Tahoe blage responses to disturbance gradients. Can. J. Fish. Aquat. and other western habitats by the copepod, Skistodiaptomus Sci. 51: 2435–2447. pallidus (Herrick) (Calanoida). Southwest. Nat. 26: 82–83. Stemberger, R., and Miller, E. 2003. Cladoceran body length and Carter, J.C.H., Dadswell, M.J., Roff, J.C., and Sprules, W.G. 1980. Secchi disk transparency in northeastern U.S. lakes. Can. J. Fish. Distribution and zoogeography of planktonic crustaceans and Aquat. Sci. 60: 1477–1486. dipterans in glaciated eastern North America. Can. J. Zool. 58: ter Braak, C.J.F. 1986. Canonical correspondence analysis: a new 1355–1387. eigenvector technique for multivariate direct gradient analysis. Case, T.J., Holt, R.D., McPeek, M.A., and Keitt, T.H. 2005. The Ecology, 67: 1167–1179. community context of species’ borders: ecological and evolu- ter Braak, C.J.F., and Šmilauer, P. 2002. CANOCO reference manual tionary perspectives. Oikos, 108: 28–46. and CanoDraw for Windows user’s guide: software for canonical Caughley, G., Grice, D., Barker, R., and Brown, B. 1987. The edge community ordination (Version 4.5). Microcomputer Power, of the range. J. Anim. Ecol. 57: 771–785. Ithaca, N.Y. Currie, D.J., Dilworth-Christie, P., and Chapleau, F. 1999. Assessing Thum, R.A. 2004. The influences of environmental differences and the strength of top-down influences on plankton abundance in incomplete reproductive isolation on parapatry in Skistodiaptomus unmanipulated lakes. Can. J. Fish. Aquat. Sci. 56: 427–436. copepods. Ph.D. thesis, Dartmouth College, Hanover, N.H. Dadswell, M.J. 1974. Distribution, ecology and postglacial disper- Torke, B. 2001. The distribution of calanoid copepods in the plank- sion of certain crustaceans and fishes in eastern North America. ton of Wisconsin lakes. Hydrobiologia, 453: 351–365. Natl. Mus. Can. Pub. Zool. 11. Webster, K.E., Kratz, T.K., Bowser, C.J., Magnuson, J.J., and Rose, Endler, J.A. 1982a. Aternative hypotheses in biogeography: intro- W.J. 1996. The influence of landscape position on lake chemical duction and synopsis of the symposium. Am. Zool. 22: 349–354. responses to drought in northern Wisconsin. Limnol. Oceanogr. Endler, J.A. 1982b. Problems in distinguishing historical from eco- 41: 977–984. logical factors in biogeography. Am. Zool. 22: 441–452. Webster, K.E., Soranno, P.A., Baines, S.B., Kratz, T.K., Bowser, Figuerola, J., Green, A.J., and Michot, T.C. 2005. Invertebrate eggs C.J., Dillon, P.J., Campbell, P., Fee, E.J., and Hecky, R.E. 2000. can fly: evidence of waterfowl-mediated gene flow in aquatic in- Structuring features of lake districts: landscape controls on lake vertebrates. Am. Nat. 165: 274–280. chemical responses to drought. Freshw. Biol. 43: 499–515. Gaylord, B., and Gaines, S.D. 2000. Temperature or transport? Williamson, C.E., and Butler, N.M. 1987. Temperature, food and Range limits in marine species mediated solely by flow. Am. mate limitation of copepod reproductive rates: separating the ef- Nat. 155: 769–789. fects of multiple hypotheses. J. Plankton Res. 9: 821–836.