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Published by THE OTTAWA FIELD-NATURALISTS’ CLUB, Ottawa, Canada
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Volume 128, Number | January—March 2014
: ; ; The Ottawa Field-Naturalists’ Club FOUNDED IN 1879 Patron His Excellency the Right Honourable David Johnston, C.C., C.M.M., C.O.M., C.M. Governor General of Canada The objectives of this Club shall be to promote the appreciation, preservation and conservation of Canada’s natural heritage; to encourage investigation and publish the results of research in all fields of natural history and to diffuse information on these fields as widely as possible; to support and cooperate with organizations engaged in preserving, maintaining or restoring environments of high quality for living things. Honorary Members
Ronald E. Bedford Michael D. Cadman Christine Hanrahan Joyce M. Reddoch Edward L. Bousfield Paul M. Catling C. Stuart Houston Allan H. Reddoch Charles D. Bird Francis R. Cook Theodore Mosquin Dan Strickland Fenja Brodo Bruce Di Labio Robert W. Nero John B. Theberge Irwin M. Brodo Anthony J. Erskine E. Franklin Pope Sheila Thomson Daniel F. Brunton John M. Gillett
2014 Council
President: Fenja Brodo Daniel F. Brunton Don Hackett Karen McLachlan-Hamilton 1° Vice-President: vacant Carolyn Callaghan David Hobden Lynn Ovenden
2" Vice-President: Jeff Skevington Barbara Chouinard Diane Kitching Rémy Poulin
Recording Secretary: Annie Bélair Owen Clarkin Diane Lepage Henry Steger
Treasurer: Ken Young Barry Cottam Ann MacKenzie Eleanor Zurbrigg
Ian Davidson
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Cover: Melanistic Maritime Gartersnake, Thamnophis sirtalis pallidulus, from Big Tancook Island, Mahone Bay, Lunenburg
County, Nova Scotia, captured on 7 May 2012. Photographed after it shed its skin in the laboratory. Photo: R. Lloyd. See pages 63-71 in this issue. 7
THE CANADIAN FIELD-NATURALIST
Volume 128
2014
Volume 128 The Ottawa Field-Naturalists’ Club Transactions
Promoting the study and conservation of northern biodiversity since 1880
THE OTTAWA FIELD-NATURALISTS’ CLUB
OTTAWA CANADA
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The Canadian Field-Naturalist
Volume 128, Number |
January—March 2014
Distribution and Abundance of Benthic Macroinvertebrates and Zooplankton in Lakes in Kejimkujik National Park and National Historic Site of Canada, Nova Scotia
CHRISTINA NUSSBAUMER!:?}5, NEIL M. BURGESS?, and Russ C. WEEBER4
Ecotoxicology and Wildlife Health Division, Environment Canada, 45 Alderney Drive, Dartmouth, Nova Scotia B2Y 2N6 Canada
“Current address: Water Survey of Canada, Environment Canada, Room 854, 220 — 4th Ave. S.E., Calgary, Alberta T2G 4X3 Canada
“Ecotoxicology and Wildlife Health Division, Environment Canada, 6 Bruce Street, Mount Pearl, Newfoundland and Labrador AIN 4T3 Canada
‘Canadian Wildlife Service (Ontario region), Environment Canada, 335 River Road, Ottawa, Ontario K1A 0H3 Canada
Corresponding author: christina.nussbaumer@ec.ge.ca
Nussbaumer, Christina, Neil M. Burgess, and Russ C. Weeber. 2014. Distribution and abundance of benthic macroinvertebrates and zooplankton in lakes in Kejimkujik National Park and National Historic Site of Canada, Nova Scotia. Canadian Field- Naturalist 128(1): 124.
As part of the Acid Rain Biomonitoring Program at Environment Canada, we sampled aquatic biodiversity in 20 acidic lakes in 2009 and 2010 in Kejimkujik National Park and National Historic Site of Canada and vicinity in Nova Scotia. We established an inventory of current aquatic macroinvertebrate and zooplankton species composition and abundance in each of the 20 study lakes. A total of 197 macroinvertebrate taxa were identified; the number of taxa observed was positively correlated with pH across the 20 lakes. Acid-tolerant taxa, such as isopods, amphipods, trichopterans, and oligochaetes, were common and abundant, while bivalves, gastropods, and leeches were lower in abundance. The number of isopods and amphipods collected was correlated with calcium concentration; a greater proportion of isopods than amphipods were collected from lakes with low calcium and low pH. Taxa with hard, calcareous shells, such as bivalves and gastropods, were not present in lakes with low calcium and low pH, with bivalves occurring only in lakes above pH 4.9. Odonates and ephemeropterans, which were low in abundance, were associated with a wide range of acidity. Coleopteran abundance was positively correlated with concentrations of dissolved organic carbon. A total of 26 zooplankton taxa were collected, but only cyclopoid abundance was correlated with lake pH. Results presented here provide a summary of aquatic biodiversity in lakes in Kejimkujik National Park and National Historic Site and vicinity and provide a baseline for future monitoring as acid deposition continues to affect this acid-sensitive region in Atlantic Canada.
Key Words: macroinvertebrates; Kejimkujik National Park and National Historic Site of Canada; water chemistry; acidic lakes: zooplankton; Nova Scotia
In the 1980s, Environment Canada implemented the Acid Rain Biomonitoring Program to study aquatic invertebrate species assemblages in acid-sensitive Bore- al Shield lakes in Ontario (McNicol et al. 1995b; Jef- fries et al. 2004). In 2009 and 2010, this biomonitoring program was expanded to include Kejimkujik National
Introduction
Acid deposition remains a widespread stressor of freshwater ecosystems across southeastern Canada de- spite legislated reductions in emissions of acidifying pollutants over recent decades in both Canada and the United States (Jeffries et al. 2004; Ginn et al. 2007).
Analyses of critical loads of acid deposition in eastern Canada have suggested regions with carbonate-poor geology continue to be influenced by acid inputs into the environment (Doka et al. 2003; Jeffries et al. 2003; Dupont et al. 2005; Clair et al. 2007, 2011). The effects of acidification on the diversity of aquatic macroin- vertebrate species have been well studied (e.g., Dermott 1985: Peterson 1987; Schell and Kerekes 1989; Lento e/ al. 2008), and changes in the composition of the aquat- ic food web can have an impact on higher trophic levels that rely on these groups for food (Weeber et al. 2004).
Park and National Historic Site of Canada, which has a long history of environmental and ecological moni- toring (Kerekes 1975; Kerekes ef a/. 1994; Burgess and Hobson 2006; Wyn et al. 2010; Clair et al. 2011).
In the period from 2000 to 2007, the Kejimkujik region in southwestern Nova Scotia received an aver- age of 8 kg « ha‘! - year! to 12 kg - ha: year of SO,” deposition (wet and dry) (Clair et a/. 2011). This level is relatively low compared to the rest of North America. However, the geology of Kejimkujik National Park and National Historic Site consists mainly of poorly weath-
i)
erable bedrock that offers little buffering capacity, and this makes this ecosystem extremely sensitive to additional inputs of acid from the atmosphere (Clair et al. 2007). In addition, the landscape in Kejimkuyjik National Park and National Historic Site and the sur- rounding area is composed of naturally acidic habitats due to the prevalence of bog and fen wetlands. There- fore, even with further reductions in atmospheric acid deposition, recovery in these aquatic ecosystems is expected to be extremely slow (Whitfield et a/. 2006; Clair et al. 2011).
Although information on the status of and trends in lake chemistry in Kejimkujik National Park and National Historic Site is well developed (Clair ef al. 2011), only limited research has been completed on the aquatic biodiversity in these acid-sensitive lakes (Kerekes and Freedman 1989; Schell and Kerekes 1989). The purpose of this study was: (i) to determine the current composition and abundance of aquatic
Peskawa
Kilometers <t
THE CANADIAN FIELD-NATURALIST
Vol. 128
invertebrate and zooplankton in 20 acid-sensitive lakes in Kejimkujik National Park and National His- toric Site and vicinity and (ii) to identify potential indicator taxa with respect to biological responses to lake acidity.
Study Area
Kejimkujik National Park and Historic Site is a pro- tected area of 404 km? located in southwestern Nova Scotia (Figure 1). Twenty study lakes (17 within the Park and 3 in the vicinity) were selected to cover a range of water chemistry parameters. Lakes were cho- sen to cover the largest possible gradients of acidity/ alkalinity, calcium, colour, and concentration of dis- solved organic carbon in the study area. All of the 20 lakes were accessible by road or canoe (some back- country lakes in Kejimkujik National Park and His- toric Site are not accessible by road, so accessibility was also a factor). Eight of the lakes were sampled in
‘ Kejimkujk National Park \. Land National Historic Site}
4 lakes sampled June 2010 se
@ lakes sampled June 2009 (n=8)
yew
FIGURE 1. Location of 20 acid rain biomonitoring study lakes sampled during 2009 and 2010 in Kejimkujik National Park and National Historic Site of Canada and surrounding area, Nova Scotia.
2014
June 2009 (Beaverskin, Big Dam East, George, Graf- ton, North Cranberry, Pebbleloggitch, Peskawa, and Puzzle) and the remaining 12 lakes were sampled in June 2010 (Back, Ben, Big Dam West, Big Red, Don- nellan, Frozen Ocean, Menchan, McGinty, Peskowesk, Snake, Turtle, and Upper Silver).
Methods Sampling methods
As part of an Environment Canada lake monitoring network, surface water samples were collected by hel- icopter from the centre of each lake during the spring and fall turnover periods each year (usually May and October) (Clair et al. 2011). Samples were collected at a depth of 0.5 m, kept cool, and shipped overnight to the Environment Canada Atlantic Laboratory for Environmental Testing (ALET) in Moncton, New Brunswick. At every 10th lake, triplicate samples were collected and compared to each other for quality con- trol. All water samples were analyzed in the laboratory for various water chemistry parameters using unfiltered water following ALET protocols (Clair et a/. 2011; Eaton et al. 2012).
For the collection of aquatic macroinvertebrates and zooplankton, we followed the sampling protocols of the Environment Canada Acid Rain Biomonitoring Program in Ontario and Quebec (see McNicol et al. 1995b). Sampling was completed in mid-June, as this is a time of high invertebrate biomass and richness and it is also when local waterbirds that depend on aquatic prey to raise their young are breeding (McNicol et al. 1996).
At each study lake we conducted 10 benthic drag samples, 10 water column sweeps, and 10 hoop sam- ples, and we set 6 minnow traps (McNicol et al. 1996). All samples were taken at randomly selected sites. Ben- thic drag samples, which targeted odonates, ephemer- opterans, bivalves, and gastropods, were conducted in water less than | m in depth. A D-frame dip net (0.85 mm mesh) was dragged over the substrate for a dis- tance of 0.5 m to collect the top 1—2 cm of substrate (total sample area of 0.14 m*) (McNicol et al. 1996). If boulders or rocky substrates made benthic drag sam- pling impractical, a traveling kick and sweep sample was completed instead. For these samples, the sampler walked backwards for a distance of | m along the shoreline (maximum | m depth), kicking the bottom substrate and sweeping the dislodged detritus and in- vertebrates into the D-frame net (Rosenberg ef al. 2000).
Both the benthic drag and the travelling kick and sweep samples were processed in the same way: detri- tus in the net was thoroughly rinsed to remove fine sediments and was transferred to a sample container,
where it was first preserved with 10% buffered forma- lin for 48 hours and then transferred into 70% ethanol. Entire benthic samples were later sorted under a dis- secting microscope. All observed macroinvertebrates were removed and preserved in 70% ethanol.
NUSSBAUMER BAL, « MACROINVERTEBRATES AND ZOOPLANKTON IN KEJIMKUJIK NATIONAL PARK 3
Sweep sampling targeted nektonic invertebrates ac- tive in the water column. Sweep sampling was con- ducted in open water less than 5 m from the shore. Sam- pling was completed by sweeping through the water column in 10 consecutive ares using a D-frame dip net (0.85 mm mesh, 625 cm? capture area) over the bow of a forward-moving canoe traveling parallel to the shore- line. Each sweep described an are from the water sur- face down to a maximum depth of | m and back to the surface, and a new section of the water column was sampled with each are. Captured invertebrates were picked from the net using forceps and transferred to a sample container containing 70% ethanol.
Hoop sampling targeted trichopterans and gas- tropods. A circular hoop of coated wire (diameter of 0.64 m, area of 0.32 m?) was placed on the substrate in water <0.5 m deep. The hoop was visually searched for a total of 5 minutes, and all invertebrates observed on the surface of the substrate and vegetation were re- moved and preserved in 70% ethanol.
All benthic macroinvertebrates from hoops, sweeps, kick and sweep samples, and benthic drags were later identified to species (or lowest taxonomic level possi- ble).
Minnow traps targeted large nektonic invertebrates. Six standard Gee’s minnow traps were baited with dry dog food (Purina Puppy Chow®) and set for a total of 24 hours in near-shore sites where water depth was approximately | m. Specimens were preserved in 70% ethanol.
Zooplankton sampling was conducted at 15 of the 20 study lakes (5 of the study lakes were <2 m deep and were therefore too shallow for vertical zooplank- ton sampling to be carried out). A single vertical haul was completed at the deepest part of each lake, starting from 1 m above the sediment to the water’s surface. Samples were collected using a non-metered zooplank- ton net (80 um mesh, 26 cm in diameter). The contents of the net were rinsed into the bottom of the collection jar and then poured into a sample jar containing 33% sugared, buffered formalin. All zooplankton samples were identified to species (or lowest possible taxonom- ic level).
Data analysis
Counts from all benthic invertebrate sampling pro- cedures were pooled within each lake for the statistical analyses. The resulting data from the 20 study lakes were summarized with respect to mean, minimum, and maximum counts for each species, as well as the per- centage of lakes where a given species was observed. Rare species (n = 72 taxa) were defined as occurring in < 10% of the study lakes, while common species (n = 125 taxa) occurred in > 10% of the study lakes. The abundance and percentage composition of the most abundant taxonomic groups were determined for each lake, and boxplots where generated to show trends for individual taxonomic groups of interest. Taxonomic richness was calculated as the total number of unique taxa in each lake.
4 THE CANADIAN FIELD-NATURALIST
Associations between water chemistry parameters, as well as between the total number of macroinverte- brate taxonomic groups and lake acidity, were evaluat- ed using Spearman rank correlations. This non-para- metric method of statistical analysis was employed as some of the data did not meet assumptions of normal- ity required for Pearson’s correlations. All statistical analyses were completed using SYSTAT 13 (SYSTAT Software Inc., Chicago, Illinois).
Zooplankton data were summarized by mean den- sity (number of individuals/m*) for each of the 15 lakes, and the percentage of lakes a given species was ob- served in was also calculated.
Results
Fish were present in all 20 of the study lakes (Kere- kes 1975; Drysdale et a/. 2005). Mean water chemistry values for each lake are presented in Table 1. Many of the study lakes were oligotrophic and darkly coloured (99-202 Hazen units) due to dissolved organic com- pounds leached from nearby bogs. Mean lake pH var- ied from 4.3 (Big Red Lake) to 6.6 (McGinty Lake) (Table 1). pH and calcium concentrations were positive- ly correlated in the study lakes (r, = 0.747, P < 0.001); pH and dissolved organic carbon were negatively cor- related (7 ——0.7 IS; P= '0.001):
A total of 26 zooplankton species were observed in the study lakes, with many of the common taxa ob- served across a wide gradient of acidity (Supplemen- tary Table 1). Only the abundance of Cyclopoida was
80 Pebbleloggitch e
70
Big Dam West e Peskawa e
60
50
Number of macroinvertebrate taxa
40
30
4.5
5.0
Vol. 128
significantly correlated with lake pH (r, = 0.536, P = 0.040).
A total of 197 taxa of aquatic macroinvertebrates were observed (149 were identified to species, 38 to genus, and 10 to family) (Supplementary Table 2). The total number of taxa in each lake was positively cor- related with both lake pH (Figure 2) (r, = 0.554, P = 0.011) and calcium concentrations (r, = 0.463, P = (0.040). Taxon richness was not significantly associat- ed with dissolved organic carbon (r, = —0.390, P = (0.090). Total abundance (number of individuals of all macroinvertebrates captured in each lake) was not correlated with any water chemistry parameter.
The most abundant benthic invertebrate groups in the 20 study lakes were Isopoda, Amphipoda, Oligo- chaeta, and Trichoptera (Figures 3A and 3B). Only one species of isopod was observed (Caecidotea commu- nis), but it constituted up to 60% of the macroinver- tebrates collected in some lakes (e.g., Peskowesk Lake) (Figure 3A). The abundance of isopods (Caecidotea communis) was lower in lakes with high pH and cal- cium levels and higher in lakes with low calcium levels (Figure 4A) (r, =—0.614, P = 0.004). Amphipods were also abundant, with Hyalella azteca collected in 19 of the 20 lakes. There was a significant positive relation- ship between amphipod abundance and calcium levels (Figure 4B) (r, = 0.776, P < 0.001). The proportion of isopods relative to amphipods decreased with increas- ing lake pH and calcium, with two exceptions (Big Dam East Lake and Turtle Lake) (Figure 4C).
Dearne
Grafton
North Cranberry
e Back
Big Dam East e *
Upper Silver a
5.5 Lake pH
6.0 6.5
FIGURE 2. Total number of aquatic invertebrate taxa observed in relation to pH of 20 lakes sampled in June 2009 and 2010 in Kejimkujik National Park and National Historic Site of Canada and vicinity in Nova Scotia. Note the significant positive trend between lake pH and the number of invertebrate taxa (P = 0.005, r. = 0.36). -
5
MACROINVERTEBRATES AND ZOOPLANKTON IN KEJIMKUJIK NATIONAL PARK
NUSSBAUMER ET AL.:
2014
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Vol. 128
6 THE CANADIAN FIELD-NATURALIS1 A 100% —_ Y} wee Y (4 Bivalvia ws Z Y) ; © Gastropoda : ATI EZ 80% — bs & Coleoptera a7) a ho @ Trichoptera £ 60% = A — BIEph tera 8 EA ee phemerop 2 & Odonata Ls) “ x rr} wine ie ‘6 @ lsopoda @ t & Amphipoda S 20% £ @ Hirudinea By He © Oligochaeta 0% 1400 B Bivalvia 1200 G Gastropoda 1000 Y Ei Coleoptera @ V/, @ Trichoptera ia — ef & Ephemeroptera S 600 3 Me | Odonata < one: oe ee Pt : @ lsopoda 400 + (eed fae Es fe sa sa ee & = eS ie vor ore fart ite RAS 5S ee ier See bo oe 5; & Amphipoda 500 gl ol ea ; io ae oF hoe Be ™, e ce oR. oe a 2 Hirudinea alll Je}. lal Jat lille il 9 44 sie 7 A ae ++ ES] ES ES ESHEETS] sy 0 Oligochaeta pod ~ - > no 2 x c 28 3 Ss ot he 5 i a 2@ & £€ S a oO 8 2 £ = bs = ae Te 08 = o oa oa © Y & rt oO S| 2 a Ss = = x @a S 2 i: o ra 9 bo 5 2 5 Z ct 3 &§ 2
Lakes arranged by pH
FIGURE 3. Percentage composition (panel A) and total abundance (panel B) of various taxonomic groups sampled in June 2009 and 2010 in 20 lakes in Kejimkujik National Park and National Historic Site of Canada and vicinity in Nova Scotia. Total abundance is the total number of individuals collected per lake. Lakes are arranged from the most acidic (Big Red Lake) (pH 4.3) to the least acidic (McGinty Lake) (pH 6.6).
Lakes with high pH and calcium concentrations had a larger number of bivalves, gastropods, and leeches (Hirudinea) (Figure 5). Bivalves were observed only in lakes with pH greater than approximately 4.9, and abundance was significantly correlated with lake acidity (Figure 5A) (r, = 0.775, P < 0.001). Gastropod abun- dance was also significantly correlated with pH (Fig- ure SB) (r, = 0.539, P = 0.014). Similarly, Hirudinea abundance was significantly correlated with lake pH
(Figure 5C) (r, = 0.789, P < 0.001). No leeches were collected from lakes with pH <5.5, with the exception of a few individuals from the Erpobdellidae family cap- tured in Peskawa Lake (pH 4.8) and Peskowesk Lake (pH 5.0). In contrast, abundance of coleopterans was significantly correlated with dissolved organic car- bon (Figure 6) (r, = 0.650; P = 0.002), but not with pH or calcium (P > 0.05).
2014 NUSSBAUMER ET AL.: MACROINVERTEBRATES AND ZOOPLANKTON IN KEJIMKUJIK NATIONAL PARK ,
150 , A) Caecidotea communis
120
Abundance WH ro)
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Abundance fon) =|
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40%
20 %
Percentage composition
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‘ isopod Caecidotea communis (panel A), the amphipod Hyalella azteca (panel B), and the corre- pare pepe apenas these two species (panel C) observed in 20 lakes sampled in June 2009 and 2010 in Kejimkujik National Park and National Historic Site of Canada and vicinity in Nova Scotia. Lakes are arranged by level of calcium from the lowest (Ben Lake) (0.18 mg/L) to the highest (McGinty Lake) (1.12 mg/L). For panels A and B, the horizontal line indicates the median, ® indicates mean, box indicates 25th and 75th percentiles, whiskers ‘ndicate minimum and maximum data points within 1.5 « the box height from the bottom or top (respectively), and
asterisks mark outliers.
8 THE CANADIAN FIELD-NATURALIST Vol. 128
A) Bivalvia
80
B) Gastropoda
Abundance
C) Hirudinea
15
10
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Lakes arranged by increasing pH
FiGure 5. Abundance of Bivalvia (panel A), Gastropoda (panel B) and Hirudinea (leeches) (panel C) in 20 lakes sampled in June 2009 and 2010 in Kejimkujik National Park and National Historic Site of Canada and vicinity in Nova Scotia Lakes are arranged from the most acidic (Big Red Lake) (pH 4.3) to the least acidic (McGinty Lake) (pH 6.6) Hori- zontal line indicates the median, ® indicates mean, box indicates 25th and 75th percentiles, whiskers indicate mini-
mum and maximum data points within 1.5 x the box height from the bottom or top (respectively), and asterisks mark outliers. ‘
2014 Nt
150
100
50
Abundance of Coleoptera
SBAUMER ET AL.: MACROINVERTEBRATES AND ZOOPLANKTON IN KEJIMKUJIK NATIONAL PARK 9
Lakes arranged by increasing dissolved organic carbon concentration
FIGURE 6. Abundance of Coleoptera in 20 lakes sampled in June 2009 and 2010 in Kejimkujik National Park and National Historic Site of Canada and vicinity in Nova Scotia. Lakes are arranged by concentration of dissolved organic car- bon from the lowest (Beaverskin Lake) (2.8mg/L) to the highest (Big Red Lake) (19.5mg/L). Horizontal line indi- cates the median, ® indicates mean, box indicates 25th and 75th percentiles, whiskers indicate minimum and maxi- mum data points within 1.5 x the box height from the bottom or top (respectively), and asterisks mark outliers.
Discussion
We found that both pH and calcium were signifi- cantly correlated with the number of aquatic macroin- vertebrate taxa observed in the study lakes. Lakes that were less acidic and lakes with higher calcium con- centrations tended to have greater species richness. These findings are consistent with other studies, which also reported fewer aquatic invertebrate taxa in more acidic lakes (McNicol et al. 1995a; Doka et al. 1997). However, the relationship between chemical conditions and the abundance of macroinvertebrates was less clear.
Fish were present in all of the study lakes (Kerekes 1975; Drysdale et al. 2005), and the presence of fish likely influenced the macroinvertebrate and zooplank- ton species richness. The most frequently collected taxa were isopods, amphipods, and trichopterans. Gastro- pods, bivalves, and ephemeropterans, commonly con- sidered to be more sensitive to acidity, were collected less frequently during the study. Lakes with lower pH had fewer taxa (consisting mostly of isopods, coleopter- ans, and oligochaetes), while lakes with higher pH had
greater taxa richness.
Isopoda and amphipoda } Only one species of isopod was collected (Caeci-
dotea communis), but this species was present in all 20
study lakes. Caecidotea communis was also the most abundant taxon in many of the study lakes, comprising > 30% of the macroinvertebrates collected in 11 of the lakes. The abundance of this species was negatively correlated with calcium concentrations, and the high- est numbers were found in the most acidic lakes (e.g., Peskawa Lake, Ben Lake, Peskowesk Lake). Schell and Kerekes (1989) also reported Isopoda in Nova Scotia lakes with pH as low as 4.4.
Isopods are known to be acid tolerant (Merritt eg al. 2008), but their high frequency of occurrence in lakes in this study contrasts with their relative rarity in lakes monitored in Ontario (RCW e7¢ a/., unpublished data). Potential explanations include differences in the species found in the two datasets (Ontario isopods were iden- tified only to order), regional differences in species habitat affinities, or a relative dominance of substrate type or other habitat conditions that encourage isopod abundance in lakes in this study area. Because sam- pling methods were similar in the two regions, we do not believe sampling variation is likely to be respon- sible for these differences.
Amphipods were also common, and their abundance was greater in lakes with high pH and high calcium concentrations. Two species of amphipods were col-
10 THE CANADIAN FIELD-NATURALIST
lected: Crangonyx richmondensis (collected in 55% of study lakes) and Hyalella azteca (collected in 95% of study lakes). In this study, 17. azteca was present across a broad pH range (i.e., 4.3 to 6.6). Studies in Ontario have identified this species as acid sensitive (McNicol et al. 1995a), with a minimum pH threshold of 5.6 or higher (Stephenson ef al. 1986; Rosenberg ef al. 1997; Snucins 2003). In this study, however, H. azteca ap- peared to be very acid tolerant and was observed in lakes with pH as low as 4.3.
Peterson (1987) also observed Hyalella in lakes with low pH (4.5—S.5) in Nova Scotia and New Brunswick, and reported that Hyalella species in lakes in the Mar- itimes appear to be more tolerant of acidic conditions than other Amphipoda. However, the lakes in that par- ticular study had higher concentrations of calcium than the study lakes with low pH in southwestern Nova Sco- tia or in acidified lakes in Ontario (Peterson 1987). The lakes in this study with low pH also had low calcium concentrations.
It may be possible that a localized population of H. azteca has adapted to the acidic environment in the lakes in Kejimkujik National Park and National His- toric Site. A genetic study by Witt and Hebert (2000) examined populations of H. azteca from various loca- tions across North America and found a complex of at least seven species rather than a single species as pre- viously believed. Grapentine and Rosenberg (1992) also suggested that populations of H. azteca may have adapted to acidic conditions in some regions of Canada.
Interpretation of regional variation in 1. azteca habi- tat associations and identification of their potential role in biological monitoring of lakes in this study area would benefit from an improved understanding of the geographic variation in their genetic profile and the consequences for their tolerance of acidic conditions.
When we compared the relative proportions of iso- pods and amphipods across the 20 study lakes, we found that isopods were dominant in lakes with low pH and low calcium concentrations while amphipods were dominant in lakes with high pH and high calci- um concentrations. Both amphipods and isopods are photosensitive and avoid bright light by moving into crevices or under rocks, leaves, and roots (Covich and Thorp 2001, page 791), where they are less exposed (complex substrates provide protection from preda- tion by fish and crayfish) (Covich and Thorp 2001, page 791). The substrate in many of the study lakes consists of cobbles and boulders, which may partially explain the high abundance of these two taxa.
Bivalvia and gastropoda
Invertebrate taxa with hard, calcareous shells such as bivalves and gastropods were generally collected only from less acidic lakes. A total of 10 species of bivalves and 12 species of gastropods were collected. Bivalve abundance was correlated with lake pH: bivalves were observed only in lakes where pH was greater than 4.9.
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Because many lakes in the study area are acidic and have low calcium concentrations, low abundance of calcium-dependent macroinvertebrate taxa was expect- ed. Our results are consistent with a previous study of 8 acid-sensitive Nova Scotia lakes by Schell and Ker- ekes (1989), which found that bivalves did not occur below a pH of 5.0.
This exclusion of calcareous species in acidic lakes has also been noted for other acid-sensitive regions of eastern Canada (Weeber er al. 2004; Jeziorski et al. 2008). As calcium concentrations in many acidified lakes continue to decline (Jeziorski et al. 2008), this may further reduce the abundance and distribution of calcium-rich taxa such as bivalves and gastropods in lakes in the study area.
Gastropods were also generally more abundant in lakes with high pH and high calcium concentrations; this finding is consistent with results from Ontario (Bendell and McNicol 1993). One exception to this is Ferrissia fragilis, which was the only species collect- ed in lakes in the study area with pH lower than 6. Bendell and McNicol (1993) also reported Ferrissia as an acid-tolerant gastropod in study lakes in Ontario, where it was the only gastropod taxon observed in lakes with pH below 6. That study also suggested that, above the minimal pH thresholds, gastropod abun- dance in small oligotrophic lakes was not limited by acidity or calcium concentrations but rather by food re- sources. Predation, substrate type, and macrophyte bio- mass can also play a large role in gastropod distribu- tions (Brown 2001, page 310). In our study lakes, the abundance of Ferrissia fragilis also did not appear to be associated with pH, calcium, or dissolved organic carbon and thus is likely limited by some other con- straint such as predation or availability of food re- sources.
Hirudinea
A total of 12 species of leeches were collected from the study lakes, with only 4 of those species being com- mon (i.e., occurring in >10% of the lakes). Counts were generally low, and abundance was correlated with lake pH. Hirudinea were not observed in lakes with pH <5.5, with the exception of two Mooreobhdella fervida collected in Peskawa Lake (pH 4.8) and one Erpob- della punctata collected in Peskowesk Lake (pH 5.0).
Bendell and MeNicol (1991) observed similar reduc- tions in the diversity and abundance of Hirudinea in acidic conditions below pH 5.5. However, they sug- gested that acidity alone does not predict the distribu- tion of leech species and that predation and availability of suitable prey also influenced their distribution (Ben- dell and McNicol 1991). In addition, other studies have shown that, although leeches are sensitive to low pH, their occurrence and abundance are also influenced by other factors, such as lake productivity (Schalk et al. 2001). Lakes in Kejimkujik National Park and Nation- al Historic Site are oligotrophic and generally have low
2014
productivity (especially at the lower pH range), and lower abundance of preferred prey may therefore play an important role in the distribution of leeches there. Coleoptera
Although lower in abundance than other groups, coleopterans appeared to be tolerant of acidity and were collected in all 20 study lakes. A total of 14 taxa were observed (8 were common and 6 were uncommon). The abundance of this taxonomic group was correlated with dissolved organic carbon. A study of Ontario lakes by Lento er al. (2008) also suggested a strong correla- tion between macroinvertebrate abundances and dis- solved organic carbon, especially in acidic lakes. Wood et al. (2011) reported that dissolved organic carbon can protect against the deleterious effects of low pH on organismal function via physiological mechanisms. Dissolved organic carbon can alter the permeability of cell membranes in acidic conditions and also influence transport physiology (Wood et al. 2011).
Other studies have suggested that water chemistry is not as important a stressor on coleopterans as predation by fish (Bendell and MeNicol 1987; Arnott et a/. 2006). The darkly coloured water of some lakes in the study area (due to high concentrations of dissolved organic carbon) may provide coleopteran taxa with some pro- tection from predation by fish and other visual preda- tors.
Trichoptera
Trichopterans were common and taxonomically di- verse in the study lakes, with 23 of the 30 taxa occur- ring in >10% of the lakes. Trichopteran species col- lected included taxa from 10 families, with the most common and abundant families being Hydroptilidae, Leptoceridae, and Limnephilidae. The trichopterans collected in the study lakes generally had a high appar- ent tolerance to acidity, with many of the observed species occurring across a wide gradient in lake pH.
Trichoptera abundance can be strongly influenced by fish predation, and trichopterans generally associated with fishless conditions, such as the leptocerid 7riaen- odes and phryganeid Banksiola (Bendell and McNicol 1995), were rare in the study lakes. Both of these organ- isms are quite large and thus are likely to be attractive prey for insectivorous fish. In contrast, the leptocerid Nectopsyche was quite abundant. They are smaller in size and construct cases with bristling twigs or elongate sticks attached that may make them more difficult for fish to consume as prey (Wiggins 2004).
Ephemeroptera and odonata . Ephemeroptera generally had low abundance in the 20 study lakes, with a total of 10 taxa collected. This is likely due to the acidity of the lakes, as ephemeropter- ans are recognized as being sensitive to acidity (Car- bone et al. 1998). Seven of the ephemeropteran taxa were common, and 3 were uncommon. The most fre- quently collected species were Caenis diminuta and the genus Eurylophella, which have been reported to have
NUSSBAUMER E£T AL.: MACROINVERTEBRATES AND ZOOPLANKTON IN KEJIMKUJIK NATIONAL PARK 1]
at least some tolerance to acidity (Carbone ef al. 1998). No ephemeropterans were collected from Ben Lake, which is low in pH (4.8) and had the lowest calcium levels of the 20 study lakes (0.18mg/L).
Odonates were taxonomically diverse in the study lakes, with a total of 30 species observed (22 species were common and 8 were uncommon). However, counts were generally low, and odonates did not make up a large proportion of macroinvertebrates in terms of abundance. The most abundant family of damselflies (suborder Zygoptera) was Coenagrionidae, which was observed across a wide gradient of acidity. Larvae in this family are relatively small (Hilsenhoff 2001, page 671) and thus may be less visible to predators such as fish or larger predatory odonates.
Within the suborder Anisoptera (dragonflies), the most common families observed in the study lakes were Cordultidae, Gomphidae, and Libellulidae, while Aeshnidae were rare. Anisoperta taxa also occurred across a wide gradient of acidity; for example, Cordu- lia shurtleffi was observed in 65% of the study lakes (pH 4.3—6.6). Bendell and McNicol (1995) also found that abundance of this particular taxon was not related to lake acidity in Ontario lakes.
Diptera
With the exception of chironomids, Diptera were not abundant in the study lakes. Ceratopogonidae were present in all 20 study lakes, and no correlation with acidity was detected. Chironomidae were frequently collected in all of the study lakes, but were not target- ed in our sampling and sorting, so specimens were not identified to species level.
Hemiptera
Very few water striders were captured in the study lakes. The only species with high abundance was Rheu- matobates rileyi, in particular in Upper Silver Lake. Although the abundance of this particular species has been shown to have a strong correlation with pH (Bendell 1988), acidity did not appear to be the main driver in the presence of this particular species in the study lakes.
Zooplankton
Of the 26 zooplankton species observed in the 15 study lakes, many were common and occurred across a wide gradient of acidity. Daphniids were the only taxonomic group that showed a clear correlation with acidity in the study lakes: they were not observed below a pH of 5.5. This finding is consistent with previous studies, which have shown daphniids to be acid sensi- tive (Yan ef al. 2008; Korosi and Smol 2012). In addi- tion, daphniids are sensitive to calcium levels (Jeziors- ki et al. 2008), and this may also explain their absence in the lakes that had low pH and low calcium concen- trations.
With the exception of daphniids, zooplankton abun- dance in the study lakes did not appear to be correlated with acidity alone. Dissolved organic carbon has been
shown to affect zooplankton populations, and the high concentrations of dissolved organic carbon in some of the study lakes may provide some protection from visual predators (Yan ef al. 2008). Using paleolimno- logical methods in 3 lakes in Kejimkuyik National Park and National Historic Site, Korosi and Smol (2012) found that there was a more pronounced change in- duced by acidification in the assemblage of cladocer- ans in clearwater lakes with lower concentrations of dissolved organic carbon over time than in assemblages in dark water lakes with more dissolved organic carbon. Zooplankton can also be influenced by a large vari- ety of natural factors, such as the availability of food, competition with other zooplankton species, the pres- ence of parasites, and the presence of both vertebrate and invertebrate predators (Yan et a/. 2008).
Future directions and conclusions
These results provide a summary of the aquatic mac- roinvertebrate and zooplankton assemblages in acid- sensitive lakes in Kejimkuyik National Park and Nation- al Historic Site and surrounding area in southwestern Nova Scotia. Although some of the overall trends of macroinvertebrate species richness with respect to vary- ing pH were similar to results reported in other regions of eastern Canada, several differences were noted.
Some of the lakes in the study area had physical characteristics that differed from acid-sensitive lakes in other regions of eastern Canada, and these physical characteristics influenced the type and abundance of benthic macroinvertebrates that were collected. pH can vary spatially within each lake as well as seasonally due to runoff, with pulses of acidity in the spring and fall (Clair et al. 2007). These pulses also coincide with lower temperatures, and at these times of the year organisms may be less active and therefore more toler- ant of their acidic environment (Stephenson and Mack- ie 1994). Although benthic microhabitats near the lake bed can have lower acidity than the upper water column (Grapentine and Rosenberg 1992), lakes in the study area are shallow with a large surface area which often allows for mixing throughout the open-water period. Therefore, benthic organisms would likely be exposed to high acidity throughout the active growth period in the summer.
All aquatic sampling methods have inherent biases in their sampling efficiencies for different invertebrate taxa. We employed multiple sampling methods in order to collect a wide range of taxa, but there was likely to have been variation in efficiency among the sampling methods with respect to particular taxa. Because the same suite of methods was used in all lakes, we assume the effects of this variation were consistent across the 20 study lakes, and we emphasize comparisons of in- vertebrate taxa patterns between lakes, rather than with- in lakes.
Our sampling methods, which were initially devel- oped to collect benthic invertebrates from thick organic sediments in small Boreal Shield lakes in Ontario
THE CANADIAN FIELD-NATURALIST
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(MeNicol e¢ al. 1995b), may not be have been as suit- able for lakes with rocky substrates. Although regional variation in species’ habitat affinities may have con- tributed to particular differences between the findings from this study and reports from other regions (€.g., isopods, H. azteca distributions), substrate or other dif- ferences in the habitat also may have been a factor. Hoop sampling (visual searches in a confined area along the shoreline) worked particularly well in our lakes for sampling species of Trichoptera. Future stud- ies should incorporate traditional benthic drag sampling with other methods such as kick and sweep, rock pick- ing, or artificial substrates.
Carbone et al. (1998) successfully sampled macro- invertebrates in shallow, rocky littoral habitats using substrate cages filled with native rocks to match the rocky littoral substrate of sample lakes. This method might work well in Kejimkuyik National Park and Na- tional Historic Site, where the littoral zone of many lakes is extremely shallow and consists of cobble and boulders. Many species collected in the study were rare (occurring in only one or two of the lakes) and had low counts. Increasing sampling effort, especially in the large lakes with varying substrate types, would reduce the likelihood of missed taxa.
Another interesting difference between the lakes in Kejimkujik National Park and National Historic Site and the lakes in the Boreal Shield in Ontario is the high concentration of dissolved organic carbon due to natu- rally occurring bogs and wetlands in the watersheds. The extremely dark waters of some lakes in the study area may benefit particular invertebrate species through physiology, protection from visual predators, or other reasons.
The data presented here establish a baseline for future monitoring in Kejimkujik National Park and National Historic Site as acid deposition continues to affect this region. Because the lakes are naturally acidic and are extremely vulnerable to additional acid inputs, recovery is slower than in other regions in eastern Canada affected by acid deposition (Clair et a/. 2011). Additional effort may be required to reduce the impacts of acidification on the aquatic organisms that live in these ecosystems.
Acknowledgements
This study was funded by the Clean Air Regulatory Agenda (CARA) program of Environment Canada. Collections were made under scientific permits from Parks Canada and Fisheries and Oceans Canada. All animal handling followed procedures approved by the Environment Canada Animal Care Committee. We would like to thank Bohdan Bilyj (BIOTAX), who completed taxonomic identifications of macroinver- tebrates, and the Sudbury Freshwater C 0-op Unit at Laurentian University, where zooplankton identifica- tions were completed. In addition, we thank Tom Clair and colleagues in the Water Science and Technology
2014
Directorate, Environment Canada for providing water chemistry data. We thank Adam Martens and Miriam Morgan for field and lab assistance. Logistical support was provided by staff at Kejimkujik National Park and National Historic Site, Parks Canada.
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Wood, C. M., H. A. Al-Reasi, and D. S. Smith. 2011. The two faces of DOC. Aquatic Toxicology 57(12) 2449-2464. Wyn, B., K. A. Kidd, N. M. Burgess, R. A. Curry, and K. R. Munkittrick. 2010. Increasing mercury in yellow perch at a hotspot in Atlantic Canada, Kejimkujik National Park. Environmental Science and Technology 44: 9176-9181.
Yan, N. D., K. M. Somers, R. E. Girard, A. M. Paterson, W. Keller, C. W. Ramcharan, J. A. Rusak, R. Ingram, G. E. Morgan, and J. M. Gunn. 2008. Long-term trends in zooplankton of Dorset, Ontario, lakes: the probable interactive effects of changes in pH, total phosphorus, dis- solved organic carbon, and predators. Canadian Journal of Fisheries and Aquatic Sciences 65: 862-877.
Received 30 August 2012 Accepted 20 February 2013
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An Illustrated Key to the Mandibles of Small Mammals of Eastern Canada
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DOMINIQUE FAUTEUX!4, GILLES LUPIEN2, FRANCOIS FABIANEK?, JONATHAN GAGNON!, MARION SEGuy!, Louis IMBEAU! Vy Bea ey 3 . . P ~ . Chaire industrielle G RSNG-UQAT-UQAM* en amenagement forestier durable and Centre d’étude de la forét, Université du wn, 4 Quebec en Abitibi-Témiscamingue, Rouyn-Noranda, Québec JOX SE4 Canada “Ministere du Développement durable, de l'Environnement, de la Faune et des Parcs, Direction régionale du Saguenay-Lac
Saint-Jean, Jonquiére, Québec G7X 8L6 Canada 3 37 ~ an P a . , . A P, ° ae - - ps entre d etude de la forét, Faculté de foresterie, géographie et geomatique, Université Laval, Québec, Québec G1 V 0A6 Canada Corresponding author: dominique.fauteux. | @ulaval.ca
Fauteux, Dominique, Gilles Lupien, Francois Fabianek, Jonathan Gagnon, Marion Séguy, and Louis Imbeau. 2014. An illustrated key to the mandibles of small mammals of eastern Canada. Canadian Field-Naturalist 128(1): 25-37.
Skulls are often used to identify small mammals, and most identification keys to small mammals have been developed on the assumption that whole skulls will be available. However, the skulls of small mammals are seldom found intact in predator pellets or nests, and the bones of several individuals are often scattered and mixed, making counting impossible without the use of a specific cranial part. In addition, only a few keys include all the species found in the eastern provinces of Canada.
Mandibles readily resist degradation by the gastric acids of both avian and mammalian predators and are often found intact in food caches of mustelids and in bat hibernacula. We therefore designed an illustrated dichotomous key to small mammals (mean mass <5 kg) of eastern Canada based on diagnostic mandible characters (including the teeth and one dentary bone). We identified and confirmed diagnostic characters to distinguish 55 species from the orders Lagomorpha, Rodentia, Sorico- morpha, Carnivora, and Chiroptera. These diagnostic characters are based on a review of the literature and were confirmed by measurements performed on both museum and trapped specimens. In order to facilitate identification, photographic illus- trations are provided for each couplet of the key.
The ability to identify small mammals using their mandibles will reduce the number of skull components needed and has proven to be a useful tool in the study of the diet of predators. This key may also be helpful in identifying bats in the genera Myotis, Perimyotis, and Eptesicus, which are presently affected by the spread of white-nose syndrome (caused by Pseudogymnoascus destructans) throughout the eastern part of Canada.
Key Words: Lagomorpha; Rodentia; Soricomorpha; Carnivora; Chiroptera; shrews; moles; voles; lemmings; mice; bats; hares; weasels; lower jaw; skull; dentary; eastern Canada
Introduction
Small mammals consumed by predators are partic- ularly difficult to identify because their skulls are often physically damaged or they have been degraded by gastric acids (Mayhew 1977). Cranial bones that resist degradation often disassociate from the larger com- ponent they were affixed to and are often found scat- tered in predator scats, pellets, or nests (Buidin et al. 2007; Khalafalla and Iudica 2010). They may also be found as concentrations of loose bones near caves or other shelters used by predators (Buden 1974). Preda- tors such as mustelids have “food caches” in which they store carcasses for later consumption (Oksanen ef al. 1985). As a result, prey remains may be disassoci- ated and may accumulate.
Several published keys to small mammal skulls are based on the assumption that the whole skull is avail- able (van Zyll de Jong 1983; Glass and Thies 1997; Lupien 2001, 2002; Nagorsen 2002; Chapman ef al. 2007), but this is rarely the case with prey remains (Mollhagen et al. 1972; Buden 1974; Balciauskiene ef
al. 2002). Furthermore, loose bones of different indi- vidual prey items are often mixed. The minimum num- ber of individuals is a derived unit of abundance often used in paleozoology (Lyman 2008). By using a single skull component, this method avoids overestimating species abundance in bone aggregations. The mandible has been proposed as a useful cranial component for identifying groups of mammals (Roest 1991; Balci- auskiene ef a/. 2002), but it has rarely been used to identify mammals to the species level, except for shrews (Repenning 1967; Carraway 1995).
The mandible, or lower jaw, is composed of teeth and a pair of dentary bones (Figure 1). The teeth of the mandible are often referred to as the lower dentition, and each tooth is identified with a lower case letter (1.e., p3 for the third premolar). For the present arti- cle, we focused on the mandible and thus omitted the term “lower”. Because the left and right dentary often separate as a result of degradation, it is imperative that the same dentary bone (1.e., left or right, but not both) be used for counting purposes.
26 THE CANADIAN FIELD-NATURALIST
Several diagnostic characters make the mandible an ideal tool for identifying most mammalian species that have very few but sturdy bones. The size, the dental formulae, and the occlusal patterns of the molar enamel are key characteristics that are often used in keys to skulls (Repenning 1967; Glass and Thies 1997; Lupien 2002; Nagorsen 2002). Furthermore, diagnostic char- acters of the dentary bones are found on both the ante- rior and the posterior parts. The size and shape of the lower edge of the ramus and the position of the mental and dental foramina, as well as the size and shape of the condylar, coronoid, and angular processes, are useful characters requiring only a few metric measurements (Roest 1991; Carraway 1995).
We present an identification key to the mandibles of all established small mammals (mean mass of <5 kg) of eastern Canada to assist in the identification of prey remains and other types of loose bones when skulls are incomplete or damaged. Each criterion mentioned in the couplets of the key is illustrated by a picture as a visual support. A glossary and the general nomencla- ture are also provided.
Methods
According to Merritt (2010), mammals may be cat- egorized as small when the average mass of the species is less than 5 kg. Based on this criterion, we selected all the small mammals established in the provinces of Ontario, Quebec, Newfoundland and Labrador, Prince Edward Island, New Brunswick, and Nova Scotia (Peterson 1966; Banfield 1974; Dobbyn 1994; Des- rosiers et al. 2002; Naughton 2012). The general tax- onomy used in the key is listed in Table 1.
This key summarizes all diagnostic mandible char- acters that we have found in the literature for the orders Lagomorpha (Roest 1991), Rodentia (Klingener 1963; Phillips and Oxberry 1972; Grayson ef al. 1990; Roest 1991; Lupien 2002; Chapman ef al. 2007), Sorico- morpha (Hallet 1978; Yates and Schmidly 1978; van Zyll de Jong 1983; Carraway 1995; Glass and Thies 1997; Lupien 2001), Carnivora (Roest 1991; Glass and Thies 1997), and Chiroptera (Gaudin et al. 2011). Cer-
Vol. 128
tain species were very difficult to distinguish using the morphologic features of the mandible alone. Therefore, we included morphometric measurements such as the length of the mandible, the length of the mandibular tooth row, and the height of the coronoid process when two species or groups of species could be distinguished only by size.
We validated the mandible characteristics presented in this key by studying specimens from Ontario, Que- bec, Newfoundland and Labrador, Prince Edward Is- land, New Brunswick, and Nova Scotia preserved in the Canadian Museum of Nature and Université Laval. Morphometric measurements were validated on 10 specimens of each species when possible. Otherwise, all specimens available were used. We further extract- ed a sample of reference mandibles from complete frozen specimens, in collaboration with the Ministere du Développement durable, de l’Environnement, de la Faune et des Parcs du Québec and the Université du Québec a Rimouski, and from specimens trapped dur- ing a related study (Fauteux et al. 2012). The relevance of the diagnostic characters in identifying prey remains was validated by Séguy (2010) using nest remains to quantify the diet of Northern Saw-whet Owls (Aegolius acadicus).
Results and Discussion
We found that 55 of the 60 small mammal species of eastern Canada could be identified from their man- dibles. The White-footed Mouse (Peromyscus leuco- pus) and the Deer Mouse (P. maniculatus) could not be identified to the species level, because their mandibles are identical. Although both Peromyscus species may be differentiated using several skull measurements, biochemical and genetic markers are probably the only reliable methods to date (Aquadro and Patton 1980; Rich et al. 1996). Similarly, three species of lagomorphs (i.e., Lepus arcticus, L. europaeus, and L. townsendii) could not be distinguished using the mandibles alone.
Consulting species’ distribution may facilitate iden- tification of small mammals (Banfield 1974: Desrosiers et al. 2002; Naughton 2012). For example, Sciurus
FIGURE I. (A. Labial view; B. Occlusal view) The mandibles of carnivores (Martes americana) (A) and rodents (Ondatra zibethicus) (B). Labels refer to the incisor (i), canine (c), premolar (p), molar (m), mandibular tooth row (mt), coronoid process (cor), condyle (con), angular process (ang), vertical ramus (vra), and horizontal ramus (Ara).
2014 Faureaux ET AL.: ILLUSTRATED KEY TO THE MANDIBLES OF SMALL MAMMALS OF EASTERN CANADA 27
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2014 FAUTEAUX ET AL.: ILLUSTRATED KEY TO THE M
niger are found only in extreme southern Ontario, and the distribution of Sorex maritimensis is restricted to New Brunswick and Nova Scotia.
The mandible is highly polymorphic between and within orders. The order Soricomorpha can be distin- guished from other orders because the canine is simi- lar in size to the premolars and the angular process is long and slender (Figure 2B) (key section D). In Lago- morpha, the large angular process and the very small coronoid process are probably the most distinctive char- acters (Figure 3A) (key section B). In contrast, species of the order Rodentia have a well-developed coronoid process, often with complex occlusal patterns on the molars (Figures 3B) (key section C). Carnivores have large canines and a coronoid process that is dispropor- tionately larger than the condyle and the angular pro- cess (Figure 4B) (key section E). Species from the order
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ANDIBLES OF SMALL MAMMALS OF EASTERN CANADA 29
Chiroptera are mainly characterized by the relatively small vertical ramus and the conspicuous bump on the lower edge of the horizontal ramus beneath the canine (Figure 5B) (key section F),
In some cases, mandibles may be broken and/or teeth may be missing. To address this problem, we pro- vide two or more criteria. However, we struggled to find more than one mandibular characteristic in cer- tain groups of species. In the orders Lagomorpha and Carnivora, only the length of the mandibular tooth row and the height of the coronoid process may be used effectively to distinguish the hares (Lepus spp.) and the weasels (Mustela spp.). Voles and lemmings may be more effectively differentiated with dental criteria, and identifications may become difficult when the teeth are missing (Banfield 1974; Lupien 2002). Although identifications using heavily degraded mandibles (e.g.,
% b
; 4 x
FiGuURE 2. (/abial view) Dentary bone of rodents with a large diastema (dia) (Glaucomys volans) (A), and soricomorphs (Blarina brevicauda) (B).
FiGurE 3. (labial view) Coronoid process (cor) and condyle (con) of lagomorphs (Lepus arcticus) (A) and rodents (Marmota
monax) (B).
ang
F g 4. (labial view) Size of the angular process as well as the size of the canine compared to the adjacent premolar in sori- IGURE 4. (Ic gul J amet ss comorphs (Parascalops breweri) (A) and carnivores (Neovison vison) (B).
30 THE CANADIAN FIELD-NATURALIST
FiGurE 5. (labial view) Dentary bones of carnivores (Mustela erminea) (A) and chiropterans (Perimyotis subflavus) (B ) with the height of the condyle (/,,,), height of the coronoid process (/,,,,.), and the conspicuous mandibular bump of chiropterans.
complete absence of teeth on specimens of Cricetidae) may be generalized, the resistance of mandibles to degradation and the number of criteria we included in the key should prove useful in identifying lightly de- graded mandibles to the species level.
Sex and age are important factors that may mean that certain mandible criteria may not be useful (be- cause of sexual dimorphism and growth). We acknowl- edge that this may be a limitation to a key based on osteometry. Identifications conducted on bones of juve- niles that are mixed with bones of adult prey may have a lower resolution (i.e., identifications stop at the genus level) than when only adults are present. As a solution, we included in the vast majority of couplets one or more known morphologic characters that are persistent through age and that do not differ between males and females, such as the morphology of the ramus. Using the mandible is also a useful tool for the counting of individual remains and do not necessitate lengthy and costly methods that often require advanced laboratory skills (e.g., identifications using DNA).
This is a new tool for identifying and monitoring all of the small mammals of eastern Canada. To our knowledge, this is the first comprehensive key designed in North America that uses the mandible exclusively. Use of the mandible enables degraded specimens of most small mammals to be identified down to the spe- cies level and it facilitates counting activities. More- over, bats of the genera Myotis, Perimyotis, and Eptesi- cus have declined dramatically in the past few years as a result of the spread of white-nose syndrome (caused by Pseudogymnoascus destructans) in the eastern part of the United States and Canada (Blehert et al. 2009). Identifying mandibles on the floor of caves and in other hibernacula might be useful for monitoring car- casses.
Acknowledgements
Financial support was provided by the Natural Sci- ences and Engineering Research Council of Canada (NSERC) and the Fonds de recherche du Québec — Nature et technologies (FRQNT) of Quebec. We thank the Centre for Forest Research and the Conseil de re-
cherches en sciences naturelles et en génie du Canada — Université du Québec en Abitibi-Témiscamingue— Université du Québec a Montréal (CRSNG-UQAT- UQAM) Industrial Chair in Sustainable Forest Mana- gement for technical support. We thank the Canadian Museum of Nature and Michel Gosselin and Kamal Khidas (both of the Canadian Museum of Nature) for their help with the skull collection and for providing us with a digital camera attached to a binocular. We thank David W. Nagorsen for providing constructive comments on earlier versions of the manuscript. We thank Amélie Drolet for linguistic revision of the text. We also thank all field assistants who participated in the collection of bones and the small mammal trapping campaigns.
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Supplementary material available at: http://www.canadianfieldnaturalist.ca
Received 9 January 2013 Accepted 8 April 2013
Glossary of terms
Alveolus Angular process
Anteroconid Anteromedian fold Anteroposterior length Brachydont tooth Condyle/condylar process
Coronoid process Closed triangle (of enamel) Mandibular foramen
Dentary bone
Diastema (plural: diastemata) Enamel
Horizontal ramus
Hypoconid
Hypsodont tooth
Interdenticular space Labial Labiolingual width
Length of the mandibular tooth row
Lingual Mandible Mandibular tooth row
Mental foramen Metaconid
Occlusal
Paraconid
Pigmentation Postmandibular foramen Premetaconid fold Protoconid
Re-entrant angles
Temporal fossa Vertical ramus
THE CANADIAN FIELD-NATURALIST Vol. 128
Socket in which the roots of a tooth are set (Figures 24, 25, and 28) (aly). Posterior and ventral-most bony projection of the mandible; the angular process is posterior to the coronoid process (Figures | and 24) (ang). Anterior-most cusp on the m1 of jumping mice (Figure 19) (antc). Concave fold created by the anteroconid on the anterior part of m1 (ant/). Length in the direction of the mandibular tooth row.
Closed-rooted tooth with determinate growth (Figures 22 and 23). Bony projection located on the ramus between the coronoid and the angular process (Figures | and 24) (con).
Posterior and dorsal-most bony projection of the mandible; the coronoid process is anterior to the angular process (Figures | and 24) (cor).
In rodents, the external layer of molars that forms occlusal triangular shapes (Figures 16 and 21) (c/).
Small hole located below the temporal fossa and serves as a canal for the dental nerve.
One side (half) of the mandible.
Space between two adjacent teeth (Figure 2) (dia).
The hard external layer of the tooth.
The anterior part of the dentary that supports the teeth (Figure 1B) (Ara). The most posterior cusp (Figure 24).
Continually growing tooth. The enamel typically covers most of the tooth. Teeth are rootless (Figures 22 and 23).
Space between the cusps present on the incisors of shrews (Figure 30). Next to the lips.
Length of teeth in the direction perpendicular to the mandibular tooth row.
Length of the lower tooth row (cl—m3) (Figures 1, 6, 33, 37, and 42). Next to the tongue; the interior of the mouth.
Both dentary bones, often referred as the lower jaw (ma).
All contiguous teeth of one dentary bone (mz). In Carnivora, Chiroptera, and Soricimorpha, all teeth form the toothrow. In Rodentia and Lago- morpha, premolars and molars form the toothrow.
Small hole located on the labial face of the horizontal ramus (Figure 24). Cusp posterior to the anteroconid on the lingual side of m1 in jumping mice.
The side of the teeth which meets with the opposing teeth. Anterior-most cusp on molars in lateral view (Figure 24).
Coloration of the teeth (pg). It is often dark in shrews.
Small hole next to the mandibular foramen that connects with the tem- poral fossa (Figure 30).
Small depression, resembling a trench, separating the anteroconid from the metaconid on the molars of jumping mice (Figure 19) (prm/). Middle cusp on the molars of shrews in lateral view (Figures 19 and 24).
Inward pointing angle defined by the margin of the prismatic molars in voles (Figures 16 and 21) (ra).
Large opening on the lingual side of the vertical ramus.
The posterior part of the dentary, composed of the coronoid, condylar, and angular processes (Figure 1B) (vra).
2014 FAUTEAUX ET AL.: ILLUSTRATED KEY TO THE MANDIBLES OF SMALL MAMMALS OF EASTERN CANADA 33
Key to the mandibles of small mammals of eastern Canada
(full key illustrated with pictures provided in Supplementary material available at: http://www.canadianfield naturalist.ca)
A. General key to small mammals la. Wide diastema between the incisor and molars (Figure 2A)
5 RAPE TES IRIAN, sein gd Behl Update 2 lb. No diastema between the incisor and molars (Figure 2B) ........0.0 0000 ece eu eeveeeeues 3 Di. an recat = itemcue Rae : ' Hee : 2a. Two premolars and three molars; coronoid process and condylar process not differentiated or coronoid process munute (Figure SA) ccc odes. ancacmecmsme ances aman Lagomorpha (section B) 5 2b. One premolar or none and three molars; coronoid process clearly differentiated from the condylar DIO ee RE TINS VE hoe oo sh id elastin wan ahs a Gm mie ame etes «EO ae's sf oN Rodentia (section C) 7 3a. Canines and premolars similar in size; well-developed angular process that is often the most posterior part of the dentary bone (Figure 4A) ................00005. Soricomorpha (section D) 31 3b. Canines two to three times the size of the adjacent premolar; small but robust angular process nhs Bs eae RCT aRE Pee eT AUN, MM eae Te, Caceres AT wal See 1 OL wt RES, (Figure 4B) 4
4a. The most posterior molar often much smaller than the most anterior molar; lower edge of ramus without a bump under the canine; height of the coronoid process much higher than the height of the COMIC PROCESS (RAOICS SAN) 2 oe a oe eth w tw oe RS Uk ewe a Re a Oa Carnivora (section E) 42 4b. Three W-shaped molars of similar size; lower edge of ramus with a bump under the canine; height of the coronoid process similar in size to or slightly higher than the height of the condylar process Ai Re CSN tae rete, Ue Merete hn cates ee aS ahh sm eat caairte tne wi whe MIS Nee x OS Chiroptera (section F) 50
B. Lagomorpha (Leporidae) 5a. Height of coronoid process >40 mm; length of mandibular tooth row >16 mm (Figure 6A)
GP SR a eae 9h denis ih Oe Aw hans Hash Ra vere deamR dor igitime dock Lepus arcticus, L. townsendii, L. europaeus 5b. Height of coronoid process <40 mm; length of mandibular tooth row <16 mm (Figure 6B) .... 6
6a. Mental foramen easily visible from the occlusal view (Figure 7A) re ere ce ee eee eta eee ELSE ee eee ee Sylvilagus floridanus
ace phn le BETA Cd RUA gx Le COSI NS JEL AE POOR AES HOE LT 4 SO Lepus americanus
C. Rodentia (Cricetidae, Dipodidae, Erethizontidae, Muridae, and Sciuridae) 7a. Lower edge of horizontal ramus with sharp angle under p1 (Figure 8A); angular process clearly smaller than the coronoid process; cheek teeth with closed circular patterns of enamel (Figure 8B) I i a aL i et at Rl: 8 ea He ib Rida gi dsr i ra Erethizon dorsatum 7b. Lower edge of horizontal ramus smooth; the coronoid process and the angular process are similar in size or the angular process is larger than the coronoid process; cheek teeth with triangular patterns of enamel or without clearly defined patterns .. 0.26. c cence eect eee eee e eee e es 8
8a. Angular process clearly the most exterior part of the mandible (Figure 9A); angular process about twice as wide labially as the condylar process (Figure 9A); anterior edge of the coronoid process that connects with the angular process creates a bump pointing outwards at the level of pl-m1 in the occlusal view (Figure 9B); 2-2... cece cree eee e reer een e ncn n es eseneesen aces Poe Marmota monax 8b. The condylar process or the coronoid process is the most exterior part of the mandible (occlusal view); no bumps created by the edge of the coronoid and angular processes next to pl-m1; angular
process about the same labial thickness or less than the condylar process ........-+-++eeseeeee 9 9a. Tip of the angular process clearly higher than the teeth igure LUA). as.s cone vee Ondatra zibethicus 9b. Tip of the angular process below or even with the teeth (Figure 10B) .......5....05.050ee. 10 10a. One premolar (Figure 11 A); angular process extends slightly behind the coronoid process (Figure GC i aah ROS Re ee A oho Perce tet afore anny Nee Ae Rei <ebee baba 11 10b. No premolar (Figure 11B); angular process extends well behind the coronoid process (Figure
: 18
Oy Ge Sane Pe NT AOR PUD. LE TP ry Goat TL RNAI PRT PHRMA OS 1 0.
34 THE CANADIAN FIELD-NATURALIST Vol. 128
lla. Coronoid process long; size of the notch between the coronoid and condylar processes similar in size to the notch between the condylar and angular processes (Figures 12A and 12B) .....---. 11b. Coronoid process relatively short; size of the notch between the coronoid and condylar processes clearly smaller than the notch between the condylar and angular processes (Figures 12C and 12D) ..
12a. T-shaped condylar process; angular and condylar processes equally posterior (Figure 12A) icy each ebeelad fg eo 00 44 gale Re’ dere ate aa S SE Oe eer aes eae) ae Ae Poliocitellus franklinii
12b. A-shaped condylar process; condylar process clearly the most posterior component of the ramus
CFigure. IAB ots keesioheits deg «vetavaaitig Ce Ghar aaah me arin oes Te ag ee ree 13 (3a, Léengthiofithe mandibular tooth now <5 Sime e aie eee es tie sas oie Tamias minimus [3b; Lenethotithemandibular toothrow =S-5.00m ..4¢. se ond sos seeeenae as aoreeee Tamias striatus 14a. Height of the coronoid process >17 mm; length of the mandibular tooth row >35mm ....... 15 14b. Height of the coronoid process <17 mm; length of the mandibular tooth row <35mm ....... 16
15a. Coronoid process short; notch created by the coronoid process and the condylar process appears
wide open; lower tip of the angular process appears squared (Figure 13A) ................. Sciurus niger 15b. Coronoid process longer; coronoid notch narrow; lower tip of the angular process appears rounded (igure ISB)" slsied ad aude yall dba eee Bee ae eee Sciurus carolinensis 16a. Uppermost edge of the condylar process relatively flat (Figure 14A) ........ Tamiasciurus hudsonicus 16b. Uppermost edge of the condylar process concave (Figure 14B) ................-.2.000-- 17 17a. Posterior tip of the angular process above the notch on the lower edge of the horizontal ramus (Chee Sv) i en a ee Glaucomys volans 17b. Posterior tip of the angular process below or at the same level as the notch on the lower edge of the hotizontalkrannasy @ig@une USB) ree: Samal 6 i ccscscna sve Fup io buenas ree sf Se ol dees Be Glaucomys sabrinus 18a. Molars without re-entrant angles or closed triangles (Figure 16A) ....................--. 19 18b. Molars with well-defined lingual and labial re-entrant angles (Figure 16B), often with closed triangles Oenainel(WSMREIGC): oss. ade bv oe eRe SOE eee ee oe eee 23
19a. Condylar process clearly the most posterior part of the dentary bone; coronoid process small, at about the same height as the condylar process (Figure 17A)
MeSH E fats) 3f 9 «: «6. eR oe Seige egy ee eee ee Peromyscus leucopus or P. maniculatus 19b. Condylar process slightly posterior to the angular process or about equally posterior; coronoid
process relatively long and higher than the condylar process (Figure 17B) .................... 20 20a. Molars with complex patterns of enamel loops (Figure 18A) ...............-cccceeeeeee 21 20b. Molars with simple patterns of enamel loops (Figures 18B and 18C) .................... 22
21a. Anteromedian fold present on m1; anteroconid of m1 clearly separated from the protoconid by the preprotoconid and premetaconid folds (Figure 19A) ........... ccc cc ecceeccccece. Zapus hudsonius 21b. Anteromedian fold absent on m1; anteroconid of m1 not separated or sli ghtly separated from the protoconid by the premetaconidifold (igure 19B) cc... ee. . couscc.ss see. cauean Napaeozapus insignis
22a. Molars with simple patterns of enamel (Figure 20A) ..........0. ccc eecccccccuu. Mus musculus seh coh Sir Rattus norvegicus
23a. Re-entrant angles of molars much deeper on lingual side than on labial side (Figures 21A, 21B, ANG2NC)s pata hveRds,«: 4 «x a's nn oy nied Ae Re ea Oe re pete when Soke ied ei 24
ree ee eee er ee Pk Peery ee re eI E E G 26 24a. Brachydont teeth (molars closed-rooted) (Figures 22A, 22B, 22C, 23A, and 23B); several small
closed triangles on the labial side of molars (Figure 21A) ........................ Phenacomys ungava 24b. Hypsodont teeth (molars open-rooted) (Figures 22D and 23C): one closed triangle or none on the labial side of each molar (Figures 21B and 21C) 2.1.2... cece cee cece cee ccc eccececee.. 25
2014 FAUTEAUX 27 4L.: ILLUSTRATED KEY TO THE MANDIBLES OF SMALL MAMMALS OF EASTERN CANADA 35
ser A single closed triangle on the labial side of each molar (Figure 21B) ...........: Synaptomys cooperi 25b. No closed triangle on the labial side of molars (Fi WUNS- SG) |; s9We lh es ooe aa Synaptomys borealis
26a. Brachydont teeth (molars closed-rooted) (Figures 22A, 22B, 22C, 23A, and 23B); occlusal triangles
of molars rounded and “enclosed” by the enamel borders (Figures 21D and 21E) ............... yi) 26b. Hypsodont teeth (molars open-rooted) (Figures 22D and 23C); occlusal closed triangles with sharp CpGeote eT 2G Sean IID: nc ows danauc cles PRRp os ee Oe eee oe 28 27a. Occlusal triangular shapes of enamel of m1 and m2 often connected by wide bridges; shape of the anterior triangle of m3 is typically similar to the posterior triangles (Figure 21D) ......... Myodes gapperi 27b. Occlusal triangles on m1 and m2 often connected by narrow bridges; shape of the anterior triangle of m3 often different from the other triangles (Figure 21E) .............cceeeeeeeeeee Myodes glareolus
28a. Presence of a small fold of enamel on the anterior and lingual side of m2 (Figure 21F)
Ra as ke EE ee teeter terete tenes e sees ss Dicrostonyx hudsonius 28b. Absence of a small fold of enamel on the anterior and lingual side of m2 (Figures 21G, 21H,
SERED A RIM Ree MRSA yen scl Hee aotearoa ti vate Blea RMR CLIN ra hohe SS OT RO 29 29a: Three Glosed trianpleson mh (Pigure 2G). wed. eee ies Sed. ee eee ds oat Microtus pinetorum 25>) Pive elosed tiangles on ml (Ficures 2Uhiand 201)" Phys Pe eG oe 30 SWee Two closed triangles on m2 (Figure 21H)» 222. Soot ee Fee Microtus chrotorrhinus
30b. Four closed triangles on m2 (Figure 211)
D. Soricomorpha (Soricidae and Talpidae) 31a. Teeth all white; incisors without a posterior cusp; alveolus of incisors does not extend under pre-
Hlolaes Gr tiniel aes Ci retin AN eS See a ce aids eA ate airs We a ae EA Op tae NO are alee 32 31b. Tip of teeth often with red and/or brown pigments; incisors with a posterior cusp; alveolus of incisors extends beneath the first premolar or posteriorly (Figures 24 and 25B) ..............-. 34
32a. Two incisors, no canine, and three premolars; presence of a short diastema between the second
incisor and the first premolar (Figure! 264) Yen. eee Ee I 8 Scalopus aquaticus 32b. Three incisors, one canine, and four premolars; presence of several short diastemata between the premolars (Figure 26B) or complete absence of diastemata (Figure 26C) .........-.--+++++55- 33
33a. Canine and the first three premolars separated by short diastemata; angular process long and slender; condylar process about the same height as the coronoid process or higher; coronoid process
clearly smaller than the condylar process (Figure 26B) .......--- 00 esee eee eee ees Condylura cristata 33b. Canine and first three premolars not separated by diastemata; coronoid process higher than the condylar process; coronoid larger than the condylar process ( PIgMneQ6E)i te: oie Mewes Parascalops breweri
34a. Alveolus of incisor extends slightly or substantially beneath m1; alveolus extends at the level of the m1 paraconid or posteriorly (Figure 27A) ........ 0. eee e eect eee eee ene een eee eens 35 34b. Alveolus of incisor does not extend beneath the m] paraconid (Figure 27B). 2.5.6 400. es. 36
35b. Three small cusps on the occlusal surface of the incisor; angular process long and very slender
CRicutie Zou tre Oe EE es PSE a oth es LN MURINE EOS oe Sorex hoyi 35a. One or two small cusps on the occlusal surface of the incisor; angular process relatively short and sObUst (RigmRO SEN) ©. NNT AUIS VaR Ree PAN Ta PN ee leek Ae As 94 Blarina brevicauda 36a. Mental foramen located beneath the m1 paraconid; the space between both cusps on the molars is relatively large (Figure 29A) ......--+ +++ sere reer teres peer tenet tenes eres Sorex dispar 36b. Mental foramen located beneath the m1 protoconid or posteriorely; the space between both cusps on the molars is relatively small (Figure 29B) ....cicisevevseoveverer tes eessub ener newsece 37
37a. Postmandibular foramen present (Figure 30A); deep interdenticular spaces on il (Figure 30B) ... 38 37b. Postmandibular foramen absent; shallow interdenticular spaces on il (Figure 30C) ............ 39
36 THE CANADIAN FIELD-NATURALIST Vol. 128
Sorex maritimensis
38a. Height of coronoid process <4.5 mm (Figure 24) 00... 6. sce ise see wens Sorex arcticus
38b: Height of coronoid process >4.5 mm (Fipiiie 24) 2. ied eee needed waa
39a. Height of coronoid process +4.5 mm (Figuré 24) ...0.... 0. case ested steed ena see Sorex palustris 39b, Height of coronoid process!=4.5 mm (Tisure 24) ovakt. Gait aes yas oes -Oe eters 40 40a. Heleht of coronoid process<3. 75 mm (Pismme 24) 2.2... 22. a hanes ee eee ee Sorex cinereus A0b, Height of eoronoid process =3, 75 mm (ricure 24)" 0s... sors es ae asv eyes sae ers Sorex fumeus E. Carnivora (Canidae, Mephitidae, and Mustelidae) Ala. Two molars; very small to no diastema between cl and p1; anterior part of the ramus under the Canimnennieke(Gisure STA)... . ova. case ena oeh le |e SRE eh ete Somer eie ERR ae 42 41b. Three molars; diastema between cl and p! about equal in size to p! or larger; anterior part of the . ramus under the canine Slender (Hirotnc Sie tee tr. eile cs settee? ee cient gee eet 48 42a, Four premolars) (Pieureis Ay) te ahs. trwuitl Puee. seen. oe OG aes bo aoe fae eo ee 43 Hw) Whe er PLEUNOVANS: (ELOUGE S21), <o.crys o>. aeveuarancue anesSinde sie acanks tee mata eae ee ea ee oo 43a. Length of the mandibular tooth row <38 mm; posterior mental foramen located beneath the hypoconid of p3; coronoid process relatively sharp (Figure 33A) ..............-.-.-. Martes americana 43b. Length of the mandibular tooth row >38 mm; posterior mental foramen often located beneath the protoconid of ps; coronoid process rounded (Figure 338) 7:2." o)4-s ee eee Martes pennanti 44a. Bump present on the anterior part of the horizontal ramus approximately beneath p1 (Figure 34A); pil’cleanhy smaller than m2 (FistreS4C)" 2... .. +. s+ «> s+ «aoe Beene eee nee Mephitis mephitis 44b. Absence of a bump on the anterior part of the horizontal ramus (Figure 34B); p1 larger than m2 or aboutsmmilar in size (guns SAD)? .. 06 aqnewee ctu one erie aseirees suse. Ge eee or 45 45a. p2 often with a well-developed paraconid (Figure 35A); posterior edge of the vertical ramus with a distinct convex notch between the coronoid process and the condylar process (Figure 36A)
eves 9: 9, EATERY Zee AR ep eC SokeY PORE EAL CEES Set ey See eee, eae ICES OR pee IA Se Se Neovison vison 4Sb. p2 often without a small anterior cusp (Figure 35B); posterior edge of the vertical ramus straight between the coronoid process and the condylar process (Figure 36B) ..................--00-. 46
46a. Height of coronoid process <7.1 mm; length of mandibular tooth row <10 mm (Figure 37) Jet yas ae BUOY senate gel ese. Web ANt, SHEE wet Petar: Were eee ee Be Mustela nivalis
47a. Height of the coronoid process generally <10.5 mm; length of mandibular tooth row never >16 mm (Figure 37); posterior edge of the vertical ramus between the coronoid process and the condylar process FOlLAUVElY Llav(PISMMOOA) oe. Sear aey tere oth cas cee eine ene chives piace. kes Mustela erminea 47b. Height of the coronoid process generally >10.5 mm; length of mandibular tooth row often >16 mm (Figure 37); posterior edge of the vertical ramus between the coronoid process and the condylar process With aconvex curve (Miche 3S), sink anee eee! Sop oe ObOkr ie nes oe es Mustela frenata
48a. Presence of a clearly defined step on the lower edge of the horizontal ramus anterior to the angular process; diastemata between cl and p1, between pl and p2, and between p2 and p3 (Figure COUN MRI AT Pn. Roe aie doa p98 Pte eee ees A Sinai. bak Ms Wan hiidh Uh ak WO | Urocyon cinereoargenteus 48b. Lower edge of the horizontal ramus anterior to the angular process smooth, without a step; only one diastema between cl and pl (Figtte 39) fir4..c.....0s--.ccvecsss.s5.. 49
49a. Anteroposterior length of the diastema between cl and p! smaller than p1 (Figure 40A) ... Vulpes lagopus 49b. Anteroposterior length of the diastema between cl and p1 about equal to pl or larger (Figure 40B) j
Levu Oh eee F 1 eS Dey REDE TE PAS eR HELE OOGME GE RTE hor Ae See een er ae Vulpes vulpes F. Chiroptera (Vespertilionidae)
30a. Three premolars (Migere Ani {7 5), fa ncaa eared aril ike, ices Andee he an 51 50b. Two premolars (Figure 41B) :
2014 Faureaux ET AL.: ILLUSTRATED KEY TO THE MANDIBLES OF SMALL MAMMALS OF EASTERN CANADA 37
Sia. Mandibular length >11.5 mm (Figure 42); hypoconid of p3 with lingual crest directed medially
creating a distinct himgual bales (Mgure ASA) osanio.sccacavecdscuasesecrss Lasionycteris noctivagans Sb. Mandibular length <11.5 mm (Figure 42); hypoconid of p3 without a distinct lingual bulge COSTS Dea ee ee ee eC es ae a ar
or Svea ar « or ati parent aha . . ini 1 ‘ 1
52a. p3 rectangular, anteroposterior length greater than labiolingual width (Figure 44A); mandibular lenbty pemerallycx Linon (Migured2). cscsas ccogsbdltlandnereee ia ieee fiw new date Myotis septentrionalis 52b. p3 squared, anteroposterior length approximately equal to labiolingual width (Figure 44B); fandibularilength<llinmn(Pisure 42)" te.wss < Weed 146.4) ORMdome tines) oheuwls eel | 53
53a. Mandibular length generally >10 mm; length of the mandibular tooth row generally >5.5 mm
(Figure 42) ERs ORT dee ais Wikia ee MRE Or he eee cn Mane etait ce 8 here, ae Myotis lucifugus 53b. Mandibular length generally <10 mm; length of the mandibular tooth row generally <5.5 mm
USGA? AAR Ieo teh wey oak Quer gare deen te St ek? Deel oom, ahh Dee | Myotis leibii ere DMIOLOM LENO rl 2a MO (INS AS) dey cs ces sass ee mest ss tees Shey yeh On ee be a) SEPANG E Goh oral erty Lea eso so ining d dp feat Ss 2 oa ae Pear erg eraser gr Pe 56
55a. Mandibular length >14 mm (Figure 42); rounded coronoid process much taller than cl (Figure 45A); p2 squared, with labiolingual width approximately equal to anteroposterior length (Figure 46A) ES Ca ee. ee Eee epee, ee Oe ag Cee MT, aOR ee ee a een er een Pee Eptesicus fuscus 55b. Mandibular length <14 mm (Figure 42); sharp coronoid process approximately same height as cl (Figure 45B); p2 rectangular with labiolingual width greater than anteroposterior length (Figure 46B) alan We ANON Ad av eind <ocaned arenas Seat el hues oh aie? Sea ed SIRS Sein) & pCR Spa Kiebrahop hrcelienis: Wyte: epene Me Heer gees) ay Gi 5 Lasiurus cinereus
56a. Length of the mandibular tooth row <5 mm (Figure 42); small diastemata separate i2 from 13, 13 from cl, and p1 from p2; cl approximately same height as p2 (Figure 47A) ......... Perimyotis subflavus 56b. Length of the mandibular tooth row >5 mm (Figure 42); no diastema between 12 and 13, i3 and cl, or pl.and.p2;:elitallenthan p2 (igure 47 Beda. < . .cRe & loom aye eiele saiereiely ere eee Lasiurus borealis
Characteristics of Barred Owl (Strix varia) Nest Sites in Manitoba,
Canada
Topp M. WHIKLO!:2:4 and JAMES R. DUNCAN?
'Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba R3T 2N2 Canada *Current address: 122 Northlands Pointe NE, Medicine Hat, Alberta, Canada 3Wildlife Branch, Manitoba Conservation, Box 24, 200 Saulteaux Crescent, Winnipeg, Manitoba R3J 3W3 Canada
‘Corresponding author: twhiklo@shaw.ca
Whiklo, Todd M., and James R. Duncan. 2014. Characteristics of Barred Owl (Strix varia) nest sites in Manitoba, Canada.
Canadian Field-Naturalist 128(1): 38—43.
During 2009 and 2010, nine Barred Owl (Strix varia) nest sites were located in Manitoba, Canada, and data on nest trees, nest structure, and nest site habitat were collected. Nests were located in a variety of tree species, including Balsam Poplar (Populus balsamifera), Paper Birch (Betula papyrifera), Trembling Aspen (Populus tremuloides) and Burr Oak (Quercus macrocarpa). All nests were in tree cavities, and the majority of nests were in dead trees (67%) and had lateral openings (67%). Habitat surrounding nest trees and estimated canopy cover were highly variable. Diameter at breast height of nest trees, cavity width, and cavity depth were consistent and were determined to be the most reliable indicators of nest suitability for breeding Barred Owls. We conclude that the distribution of nesting Barred Owls is influenced more by availability of suitable nest sites than by
nest tree species or nest site habitat.
Key Words: Barred Owl; Strix varia; habitat; nesting; raptor; Manitoba
Introduction
Barred Owls (Strix varia) nest in a variety of natu- ral and anthropogenic structures (Robertson 1959; Shackleford 1996; Houston 1999), but are considered to be primarily cavity nesters (Mazur et al. 1997a, 1997b). They use tree cavities created by other birds, disease, rot, and/or tree damage (Mazur ef al. 1997a; Vaillancourt et al. 2009). Because of its reliance on large diameter trees for nesting, the Barred Owl is considered an indicator species of forest health (McGarigal and Fraser 1984). The availability of nest sites limits its dis- tribution, population size, and density (Robertson and Rendell 1990).
As a highly adaptable species (Robertson 1959: Shackleford 1996), the Barred Owl persists in some habitats that have been altered by human activity (Kelly et al. 2003; Houston 1999). However, nesting require- ments must be met in order for avian populations to be maintained (Robertson and Rendell 1990). The Barred Owl’s nesting requirements are poorly documented throughout most of its range (North America) (Mazur et al. 1997a), and specifically in Manitoba (Holland e¢ al. 2003). io
Across its range, the Barred Owl uses forest types along a gradient from hardwood to mixedwood to soft- wood forests (Nicholls and Warner 1972). Hardwood forests are rare throughout a large portion of its north- ern range, leaving only mixedwood and mostly boreal forests (Duncan and Kearns 1997). The link between large cavity-nesting species and mature stands of mixed- wood forests is known (McGarigal and Fraser 1984; Potvin ef al. 2000; Hodson 2003; Payer and Harrison 2003).
Barred Owl management and conservation by the government in Manitoba and elsewhere will be more
effective if we understand which factors create suitable Barred Owl habitat within various mature mixedwood stands. Our objectives were to locate Barred Ow! nest sites in Manitoba, Canada, and collect data on nests, nest trees, and nest site habitat. Describing these factors will contribute to hypotheses about nest and habitat selection in this species and the limits to their distri- bution in Manitoba and elsewhere.
Study Area
Research was conducted from February 2009 to September 2010 within the southern portion of Mani- toba, Canada (49°0.0'N to 53°52.7'N and 95°9.2'W to 101°44.2'W). This area consists of prairie pothole, bore- al hardwood transition, boreal taiga plain, and boreal softwood shield regions (Zoladeski ef al. 1995). Pre- dominant tree species in the study area were White Spruce (Picea glauca), Black Spruce (Picea marinana), Tamarack (Larix laricina), Jack Pine (Pinus banksiana), Trembling Aspen (Populus tremuloides), Balsam Poplar (P. balsamifera), and Paper Birch (Betula papyrifera). Southern Manitoba lacks major topographic changes; however, small shifts in elevation, along with the abun- dance of wetlands and waterways, create a highly vari- able habitat (Zoladeski et al. 1995).
Methods
Barred Owl nest sites were located using nocturnal audio surveying and diurnal audio playback with pas- sive observation during the breeding season (February — June in 2009 and 2010) (Frith er al. 1997; Whiklo 2011). Survey transects were laid out in areas based on Barred Owl detection data obtained from the Manitoba Nocturnal Owl Survey (JRD, unpublished data: op. cit. Duncan and Kearns 1997) and historical accounts, and
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transects were also laid out in suitable habitat adja- cent to known areas of Barred Owl activity. In total approximately 1321 km of transect lines were surveyed in 2009 and 2010. Survey locations were situated 1.6 km apart along survey transects where playback of Barred Owl vocalizations were used to elicit responses (Whik- lo 2011). Areas where Barred Owls were detected dur- ing nocturnal surveys were searched during daylight for active nests.
Nest trees were categorized as live or dead, and tree species, the height of the nest above ground, and diam- eter at breast height (DBH) were recorded. Diameter at breast height was calculated by measuring the cir- cumference of the tree and then calculating the diam- eter: D= C /x. Cavity height (distance from the lowest point inside the nest to the highest point inside the nest), cavity width (distance from the furthest right-hand point inside the cavity to the furthest left-hand point inside the cavity), and cavity depth (distance inside the cavity perpendicular to cavity width) were measured; nest type (cavity, stick, other) and cavity orientation (lateral or apical) were also recorded.
Habitat within a 30 m circular plot surrounding the nest trees was categorized using Manitoba Forest In- ventory classifications (Zoladeski et al. 1995), and the percentage canopy cover was estimated (Whiklo 2011). All measurements are reported as mean and standard deviation (SD).
Results
A total of nine Barred Owl nests were located in 2009 and 2010 within a 25 000 km? rectangle in south- eastern Manitoba. All nests were cavity type structures; six were lateral cavities and three were apical cavities (Table 1). Six nest trees were dead and three were liv- ing (Table 1). Five nests were found in Balsam Poplar, two in Paper Birch, one in Trembling Aspen, and one in Burr Oak (Table 1). The mean nest height above ground was 7.7 m (SD 2.6). The mean diameter at breast height of nest trees was 49.2 cm (SD 18.9). The mean cavity height was 71.8 cm (SD 46.9), the mean cavity depth was 42.1 cm (SD 33.0), and the mean cavity width was 27.3 cm (SD 5.4) (Table 2).
Four nest trees were located in Balsam Poplar mixed- wood (V1) stands, two in Black Ash (Fraxinus nigra) hardwood (V2) stands, one in a White Spruce/Balsam Fir (Abies balsamea) (V21) stand, one ina Miscella- neous Hardwood (V3) stand, and one in an area that could not be classified due to a lack of living trees (a pond created by an American Beaver, Castor canaden- sis) (Table 1). The mean estimated canopy cover was
42.8% (SD 27.2) (Table 2).
Discussion . There are a considerable number of studies that ex-
amine one or more aspects of the nest site structure, the nest tree species, and/or the habitat associated with the nest sites of the Barred Owl (Nicholls and Warner 1972;
TABLE |. Data for nine Barred Owl (Strix varia) nest sites in Manitoba, Canada (2009 to 2010).
Manitoba forest classification!
Nest tree status Nest type
Nest tree species
Owl nest site
V1: Balsam poplar hardwood and mixedwood
Dead Lateral cavity
Balsam Poplar
Cow Moose Lake (Barred Owl 4)
Watson P. Davidson Wildlife
V1: Balsam poplar hardwood and mixedwood V1: Balsam poplar hardwood and mixedwood
Apical cavity N/A*
Dead
Paper Birch
5)
(=
Management Area (Barred Owl Stead (Barred Owl 11)
Dead Lateral cavity
Balsam Poplar
Dead Lateral cavity
Balsam Poplar Balsam Poplar
Otter Falls (Barred Owl 20)
V2: Black ash (White elm) hardwood V21: White spruce/Balsam fir shrub
Lateral cavity
Live Dead
Nutimik Lake (Barred Owl 27)
Apical cavity
Balsam Poplar Paper Birch
West of Woodridge (Barred Owl 31) East of Piney (Barred Owl 36)
WHIKLO AND DUNCAN: BARRED OWL NEST SITES IN MANITOBA
V1: Balsam poplar hardwood and mixedwood V2: Black ash (White elm) hardwood
V3: Miscellaneous hardwoods
Apical cavity
Dead
J
Contour area (Barred Owl
Live Lateral cavity
Trembling Aspen Burr Oak
Lateral cavity
Live
Dencross (Barred Owl 56)
*Habitat was determined to be unclassifiable according to Manitoba forest classifications due to lack of living trees.
' Zolandeski et al. (1995)
THE CANADIAN FIELD-NATURALIST
Vol. 128
TABLE 2. Further data for nine Barred Owl (Strix varia) nest sites in Manitoba, Canada (2009 to 2010). eee — ese
Nest tree Height of the
diameter at nest above Cavity Cavity Cavity Canopy
breast height the ground height depth width cover Owl nest site (cm) (m) (cm) (cm) (cm) (%) Cow Moose Lake (Barred Owl 4) 43.1 4.5 68.8 26.4 Ni fere' 30 Watson P. Davidson Wildlife
Management Area (Barred Owl 5) 42.9 7.4 24.9 B29) 29.4 39
Stead (Barred Owl 11) 50 10.2 156.0 127.0 24.5 60 Otter Falls (Barred Owl 20) 39.7 6.4 AI 22.8 26.1 0 Nutimik Lake (Barred Owl 27) 56.2 2A 67.9 35.9 35.9 70 West of Woodridge (Barred Owl 31) B34) 5.8 11.4 YS) 2S 75 East of Piney (Barred Owl 36) 33},3) 5.4 42.0 29.8 ZAR? 5 Contour area (Barred Owl 55) 48.7 7.6 102.2 30.8 35,1 50 Dencross (Barred Owl 56) 95.5 9.9 Sy) 51.0 24.0 60 Mean (SD) 49.2 (18.9) 7.7 (2.6) 71.8 (46.9) 42:1(33.0) 27.354) 42.8 (27.2)
Haney 1997; Mazur et al. 1997a, 1997b; Postupalsky et al. 1997; Winton and Leslie 2004; Olsen ef a/. 2006; Grossman ef a/. 2008; Singleton ef a/. 2010) and gen- eral Barred Owl habitat associations (McGarigal and Fraser 1984; Booth and Harrison 1997; Mazur et al. 1998; Hamer et al. 2007; Russell 2008). These studies vary considerably, as described in more detail below, in the way study areas were selected, in the size and habitat fragmentation of the study areas, and in the size and measurement of nest habitat plots. However, there is less variation in the way nest trees and nest sites were measured.
This variation in methodology limited our ability to compare results; nevertheless, some Barred Owl nest site characteristics were consistent across studies.
Nest type
In contrast to other studies (Mazur et al. 1997a;: Pos- tupalsky et al. 1997; Olsen et al. 2006), all nests (n = 9) located in the study were in tree cavities (Table 1). Mazur et al. (1997a) reported that 5 of 15 Barred Owl nests (33%) in the study in the boreal forest of Sas- katchewan were in structures other than tree cavities; in witch’s broom (the dense branching caused by Arceu- thobium spp. in a White Spruce tree), in Red Squirrel (Tamiasciurus hudsonicus) nests, or in stick nests. In a study in the boreal mixedwood forest in Alberta (Olsen et al. 2006), 9 of 10 nest sites (90%) were in tree cavities (one Barred Owl nested in a stick nest). In Michigan, in hardwood (deciduous) and mixed for- est habitat, Postupalsky er a/. (1997) described 13 of 57 nests (23%) as being open sites, including hawk (Red-shouldered Hawk (Buteo lineatus) or Broad- winged Hawk (Buteo platypterus) and Northern Gos- hawk (Accipiter gentilis)) stick nests, a ground nest, a flat area in the fork of a Yellow Birch (Betula alle- ghaniensis), and a nest platform intended for Great Horned Owls (Bubo virginianus); the remainder were in tree cavities (n = 26) or nest boxes (n = 18).
The likelihood of finding an open Barred Owl nest in Manitoba would presumably increase with increased effort and sample size. However, it is noteworthy that, even though Barred Owls are known to use artificial open nests (Olsen ef a/. 2006), none were found nesting on a cumulative total of 2527 natural and/or artificial open stick platform nests in a variety of habitats checked for raptors over a 27-year period (1984-2010) in the same 25 000 km? study area in southeastern Manitoba (Duncan 1992; JRD, unpublished data).
The aforementioned studies (Mazur et al. (1997a), Postupalsky et al. (1997), and Olsen et al. (2006)) varied considerably in the way the study areas were selected or described, in the size of the study areas, in the methods used to find nests, in the forest habitat composition/ fragmentation, and in other quantified ways (i.e., prey density, human disturbance). For example, this study was larger (~25 000 km?) with varied habitat, the study described in Mazur et al. (1997a) was conducted with- in a 3 874 km* national park, the study described in Olsen et al. (2006) was a 800 km? predetermined area, and two study areas (28 km? and an undefined larger area) were studied in Postupalsky er al. (1997).
Smaller fragmented study areas or isolated protect- ed areas (1.¢., national parks) may vary in terms of the availability of cavity nests, the prey density, the forest habitat, and/or intra and interspecific competition, re- sulting in the variation observed in the proportion of nest type use by breeding Barred Owls. How these fac- tors affect the availability of suitable cavity nest sites and the proportion of Barred Owls using open nest sites is unknown. However, the propensity of Barred Owls for cavity nests likely results from natural selection: Barred Owls nesting in cavities experience greater reproductive success than those that use open nests (Postupalsky et al. 1997).
Nest cavity characteristics
Given the importance of nest cavities to Barred Owl reproduction, we recorded a series of measurements. Cavity height and depth ranged widely (height ranged
2014
from 11.4 to 156.0 cm and depth ranged from 22.3 to 127.0 cm) with high standard deviations, whereas cav- ity width was remarkably consistent (21.2 to 35.9 em) (Table 2), despite the variation in nest tree species and Status (live or dead) (Table 1). Cavity depth varied the most, perhaps as a result of the variable and sometimes advanced stages of tree decay, e.g., the nest site near Stead (Table 2). Postupalsky ef al. (1997) recorded a similar mean cavity width (26.9 cm, range 18-44, n= 25), but did not report cavity depth measurements (as defined in this study) or standard deviations. Nest cavity measurements were not reported in other studies.
Nest tree diameter at breast height
Mean diameter at breast height of nest trees in this study (49.2 cm, SD 18.9) was consistent with that re- ported in other studies. Mazur et al. (1997a) recorded an average diameter at breast height of 47.4 cm (SD 12.8, n = 15), despite recording considerably higher values for the height of nests from the ground (13.3 m, SD 4.1) than this study (7.7 m, SD 2.6) (Table 2). Olsen et al. (2006) recorded an average diameter at breast height of 51.6 cm (SE 4.3), along with a relatively inter- mediate nest height above ground (10.4 m, SE 2.1).
There were relatively large differences in many nest tree variables among these studies (e.g., nest tree height, nest height, proportion of cavity nest structures, and nest tree species); therefore, the similarities in the diam- eter at breast height of nest trees suggest it is a valid and practical indicator of Barred Owl nest tree suit- ability. Nest tree species, percentage canopy cover, and forest stand composition
Barred Owls nested in four hardwood tree species in this study (Table 1), and this variation was similar to that found in other studies. Mazur ef al. (1997a) re- ported Barred Owl nests in both softwood (coniferous) and hardwood tree species, including White Spruce (n = 5), Trembling Aspen (n = 5), Balsam Poplar (n= A), and Paper Birch (n = 1). Olsen et al. (2006) docu- mented Barred Owl nests in fewer tree species in a smaller study area: Balsam Poplar (n = 8) and Trem- bling Aspen (” = 2). Barred Owls use a variety of nest tree species, live or dead, and they readily breed in arti- ficial nest boxes placed in a variety of trees (Postupal- sky et al. 1997). It is therefore unlikely that Barred Owls choose a nest site based on tree species per se.
High percentage forest canopy cover has been cit- ed as a determining factor in Barred Owl selection of breeding habitat, possibly because it provides solar insulation (Nicholls and Warner 1972; Haney 1997; Winton and Leslie 2004; Grossman ef al. 2008), but the influence of forest canopy may depend on the size of the area that was measured. In this study, canopy cover was measured within a 30 m circular plot cen- tered on the nest tree, and it did not appear to influ- ence Barred Owl nest tree habitat use: more than half the sample had a canopy cover of <50% (Table 2).
WHIKLO AND DUNCAN: BARRED OWL NEST SITES IN MANITOBA 4]
Mazur et al. (1997b) used a similar small-scale plot (11.3 m radius) with the nest tree at the centre, and reported a somewhat higher mean percentage cover of 57% (SD 17); this was not significantly different from random plots. Other studies reported yet higher per- centage canopy cover within larger Barred Owl home ranges: 96% (SE 1.1) (Haney 1997), 62.8% (Winton and Leslie 2004), utilized “dense” cover disproportion- ately (no values given) (Nicholls and Warner 1972), >66% (Grossman et a/. 2008), and >56% (Singleton ef al, 2010).
Forest stands within the 30 m circular plots (centered on nest trees) were classified as one of three types of stands: hardwood and mixedwood, softwood shrub, or unclassified (American Beaver pond) (Table 1). This variation in nest habitat use is reflective of the great variety of forested areas over the considerable North and Central American range of the Barred Owl, from swamps and riparian areas to upland regions (Mazur and James 2000). This variation of forest stand nesting habitat use suggests that the Barred Owl is a forest habi- tat generalist.
Management of forests for Barred Owls
Strong selective pressure on Barred Owls appears to have resulted in their propensity for nest cavities in trees. Observed higher reproductive success in cavity nests implies nest site selection for cavities by this species (Postupalsky ef al. 1997). This conclusion is supported both by our results and by those of others, in which the most consistent nest characteristics and nest habitat characteristics reported are the width of the nesting cavity and the diameter at breast height of the nest tree. Other Barred Owl nest habitat characteristics discussed herein vary considerably across the range of the Barred Owl. Apart from its effective dependence on suitable nest tree cavities, the Barred Owl is otherwise generally considered a forest habitat generalist (Mazur and James 2000).
The persistence of Barred Owl populations depends on the maintenance of forests with trees with a mini- mum diameter at breast height capable of producing cavities large enough for this large cavity-nesting species (Haney 1997). Knowledge of ecological factors and processes that promote the formation of suitable nest tree cavities is also critical to the maintenance of Barred Owls in a managed forest environment.
Barred Owls are associated with water (Mazur ef al. 1997b; Hamer et a/. 2007), mature or “old-growth” forest stands (McGarigal and Fraser 1984; Mazur ef al. 1998), and mixedwood or hardwood stands (Booth and Harrison 1997; Mazur et al. 1997b; Russell 2008).
The role and importance of heart rot in hardwood species in the formation of nest cavities, as well as the role of snags in an ecosystem, are well documented (Thomas et al. 1979; Witt 2010). Barred Owl nest cav- ities found in this study were natural and had resulted from damage to and decay of the tree. These cavities
42 THE CANADIAN FIELD-NATURALIST
were not readily attributable to excavation by primary cavity nesters.
Cavities not created by primary cavity nesters are often created by tree decay and rot (Bunnell ef al. 2002). Fungal rot is prevalent in older and/or larger stands of trees (Witt 2010) and has positive effects for both primary and secondary cavity nesters (Bunnell e¢ al. 2002). Higher levels of moisture and humidity, fac- tors found at sites within close proximity to water, in- crease the rate of decay in trees (Jackson and Jackson 2004). In Manitoba, hardwood species decay at a high- er rate than most softwood species: annual losses of hardwood species to decay are double that of softwood species (Brandt 1995).
Barred Owl conservation would benefit from the development and use of a standard methodology to characterize nest sites and nesting habitat. Standard methodology would allow the results from studies across this species’ range or through time to be com- pared. We also recommend that tree species composi- tion, diameter at breast height, and ecological forest decay indicators be developed and used to identify pri- ority Barred Owl habitat conservation areas where for- est habitat loss affects the viability of local Barred Owl populations.
Acknowledgements
This research was supported by Manitoba Conser- vation, Manitoba Hydro, the University of Manitoba, the Manitoba Model Forest Inc., the Raptor Research Foundation, and the Winnipeg Foundation. Thanks to Robert Nero and Terry Galloway for reviewing drafts of this manuscript and providing comments. We also thank the two anonymous reviewers for their helpful comments.
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Received 15 March 2013 Accepted 29 May 2013
Yellow Warblers (Setophaga petechia) Rear Second Broods in Some Years at Delta Marsh, Manitoba
SPENCER G. SEALY
Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba R3T 2N2 Canada; email: sgsealy@ec.uman itoba.ca
Sealy, Spencer G. 2014. Yellow Warblers (Setophaga petechia) rear second broods in some years at Delta Marsh, Manitoba. Canadian Field-Naturalist 128(1): 44-49.
Twenty cases of double brooding by colour-marked Yellow Warblers (Setophaga petechia) were recorded in 5 of 11 years (1975-1986, no data collected in 1977) during studies of breeding ecology in the dune-ridge forest at Delta Marsh, Manitoba (1 pair in 1975, 3 pairs in 1976, 3 pairs in 1984, 9 pairs in 1985, and 4 pairs in 1986). At least one member of each of the 20 pairs was marked. Eleven pairs re-used their first nest for the second attempt, whereas 9 females built a new nest, in 5 cases because the original nests had disintegrated. Four of the second nests (3 in 1985 and | in 1986) were parasitized by Brown-headed Cow- birds (Molothrus ater). All 20 first nests produced at least one young, a condition for double brooding, and 13 second nests, including 3 that were parasitized, were successful. Failure of about 60% of annual nesting attempts at Delta Marsh may contribute to the low number of pairs with double broods recorded in some years and the absence of double brooding in years of comparable phenology. This is the first published evidence of double brooding in the Yellow Warbler.
Key Words: double broods; Yellow Warbler; Setophaga petechia; Delta Marsh; Manitoba
Introduction but only in some years. Other workers have suspected Knowledge of the number and success of broods double brooding by Yellow Warblers, but their obser- attempted by birds in each breeding season is important vations were based on one or only a few nests attended for an understanding of the dynamics of avian popula- _ by unmarked birds (e.g., Stoner 1932; Salt 1973; Ban- tions and life history evolution (Martin 1987). One of — croft 1979). Confirmation of double brooding by Yel- the components of the life cycle is the number of broods low Warblers at the northern latitude of Delta Marsh individuals typically rear in each breeding season, suggests that double brooding may be a regular occur- whether one, two or even more in certain years when _ rence in this species’ breeding biology. conditions are suitable. This contrasts with the replace- ment of clutches and broods that may be depredated Study Area or otherwise fail, possibly due to inclement weather. Data from first and second broods of the Yellow An irrefutable determination that birds have raised Warbler were recorded from nests discovered in the one brood and attempted to raise another requires care- dune-ridge forest that separates Lake Manitoba and ful monitoring of colour-marked individuals or radio- | Delta Marsh, Manitoba, 50°11'N, 98°19"W (Goossen tracking throughout the entire breeding season. In some and Sealy 1982; MacKenzie 1982: MacKenzie et al. species, researchers have recorded double brooding in- 1982; Pohajdak 1988). Nests were monitored over 11 frequently, often as isolated cases (e.g., in the Northern _ years (1975-1986, except 1977) by J. P. Goossen (1975 Yellow-throat, Geothlypis trichas (Stewart 1953); in and 1976) and by me in the other years, although some Kirtland’s Warbler, Setophaga kirtlandii (Radabaugh __ nests in the latter years were located by co-workers con- 1971); in the Bobolink, Dolichonyx oryzivorus (Gavin ducting other studies. The number of Yellow Warbler 1984); and in the Dickcissel, Spiza americana (Bolinger nests, which included replacement nests, monitored in and Maddox 2000)), whereas others have recorded — each year of the study was: 119 in 1975, 148 in 1976, double brooding by 648% of pairs, with successful 64 in 1978, 59 in 1979, 44 in 1980, 126 in 1981. 157 in second broods increasing an individual’s annual pro- 1982, 237 in 1983, 260 nests in 1984, 225 in 1985. and ductivity (e.g., in the Black-throated Blue Warbler, 241 in 1986. Setophaga caerulescens (Holmes et al. 1992); in the Yellow Warblers investigated in this study nested in Hooded Warbler, Setophaga citrina (Evans Ogden and —_a 7-km portion of the dune-ridge forest (~80 m wide; Stutchbury 1996); and in the Louisiana Waterthrush, 56 ha), abutted by the lake on the north side and an Parkesia motacilla (Mulvihill et al. 2009)). extensive marsh of cattail (Typha latifolia) and reed During an Il-year study of breeding and feeding (Phragmites communis) on the other (see map in Sealy ecology of Yellow Warblers (Setophaga petechia) ina 1980a). This portion of the ridge forest stretched from riparian habitat at Delta Marsh, Manitoba, from 1975 the west at Cram Creek eastward along the property to 1986 (no data were collected in 1977), co-workers of the Portage Country Club to the eastern edge of the and I recorded irrefutable evidence of the rearing of — property of the Delta Marsh Field Station (University second broods after young had fledged from first nests, | of Manitoba). Yellow Warblers nested in the ridge for-
44
2014 SEALY: DOUBLE BROODING BY YELLOW WARBLERS AT DELTA MARSH, MANITOBA 45
est predominantly in Sandbar Willow (Salix interior), Manitoba Maple (Acer negundo), Red-berried Elder (Sambucus pubens), Pin Cherry (Prunus pensylvanica), Cc hoke Cherry (P. virginiana), and Red-osier Dogwood (Cornus stolinifera). Peach-leaved Willow (S. amyg- daloides), Green Ash (Fraxinux pennsylvanica), and Eastern Cottonwood (Populus deltoides) also contri- buted to the overstory vegetation in this riparian habitat, but few Yellows Warblers nested in them (MacKenzie et al. 1982).
Methods
Adults of this sexually dichromatic, seasonally mon- ogamous species (Reid and Sealy 1986) were mist- netted and colour-marked as after-hatch-year (AHY) males or females, following an annual banding pro- tocol established late in 1974 and continued in each subsequent year of the study (e.g., Sealy 1980b; Sealy and Biermann 1983). Thus the first spring in which marked individuals were present in the study area was in 1975.
In addition, males and females were opportunistical- ly captured and colour-banded near their nests (Cosens and Sealy 1986; Hobson and Sealy 1989). Colour- marking of nestlings and hatch-year (HY) individuals mist-netted prior to fall migration also began in 1975, and birds marked in that and subsequent years resulted in individuals of known age present in the study area in successive years. These individuals originally received a single coloured band, which, in combination with an aluminum band, denoted the year of hatch, so these birds became recognizable in their first spring as second- year (SY) individuals, and older in succeeding years. Upon recapture, year-marked individuals received two additional coloured bands that uniquely identified them. This marking program resulted in a sample of nests each year that were attended by at least one marked male or female (in several cases both adults were marked).
Yellow Warblers nested at densities up to 29 pairs/ha in the ridge forest in those years (Goossen and Sealy 1982: also see Sealy 1995). This density allowed dozens of nests to be discovered in most years before clutches were initiated, enabling day-to-day inspections as eggs were laid and inspections every one to four days through fledging of first and second broods. The extremely high nesting densities (Goossen and Sealy 1982), however, meant that only a small undetermined number of indi- viduals could be marked, thus precluding the determi- nation of the proportion of pairs that attempted second broods in each of the years in which double brooding was recorded.
| am confident that second broods were not attempt- ed by any pairs in the 6 years in which none were re- corded because I monitored a sample of nests, both those attended by marked birds and those attended by unmarked birds, equally diligently throughout all breed- ing seasons of the study (see Sealy 1995; Guigueno and Sealy 2010; Mazarolle e/ al. 2011).
Results
Double brooding was recorded in 20 pairs of Yellow Warblers of known age in 5 of the 11 years of the study (Table 1): 1975 (n = 1 pair), 1976 (n = 3 pairs), 1984 (n = 3 pairs), 1985 (n = 9 pairs), and 1986 (n = 4 pairs). At least one member of each pair was marked. Males (at 8 nests), females (at 5 nests), or both males and fe- males (at 7 nests) were marked, thus permitting irre- futable confirmation of double brooding (Table 1).
These data suggest that all pairs remained together during the second nesting attempt, although polygyny, albeit infrequent in this population (Sealy 1984; Reid and Sealy 1986), could have resulted in a change of mate at nests where only one of the adults was marked. This would not change the fact, however, that double brooding occurred.
Among the 20 pairs with double broods were 4 whose second clutch was parasitized by a Brown- headed Cowbird (Molothrus ater) (3 in 1985 and | in 1986). None of the first nests of these or any of the other pairs that went on to attempt to raise a second brood were parasitized (Table 1). The frequency of par- asitism by Brown-headed Cowbirds in this population of Yellow Warblers (also see Sealy 1995) was 26.1% of 119 nests monitored in 1975, 23.0% of 148 nests in 1976, 18.1% of 260 nests in 1984, 18.7% of 225 nests in 1985, and 17.8% of 241 nests in 1986.
Each pair’s first nesting attempt successfully fledged at least one young, a necessary condition for double brooding. At one of the first nests in 1985, however, incubation was delayed about 3 days while the female replaced 3 of 4 eggs that had gone missing from the original nest (footnote 3 of Table 1). Clutches at 18 of the 20 first nests (90%) were initiated by 2 June (Table 1) in years where first eggs in the population were ini- tiated on or up to 7 days before this date (also see table III in Sealy 1995).
All 7 marked pairs remained together for their sec- ond nesting attempt, lending support to the assump- tion that the members of the other pairs also did not change (although in these cases it was confirmed only that the same marked individuals (8 males and 6 fe- males) remained for the second attempt). Eleven pairs, including the 4 pairs whose second clutches were para- sitized, used their first nest for the second attempt. One female whose nest had been parasitized built a new nest over top of the one Brown-headed Cowbird and the two Yellow Warbler eggs that had been laid in the original nest. Nine females built a new nest for the second attempt (Table 1), in 5 cases because the orig- inal nests had disintegrated. The other 4 pairs built a new nest in another location nearby. None of the indi- viduals with double broods was among the pairs that double brooded in previous or subsequent years, and no young produced in first or second nests, although banded, were subsequently captured in the study area.
Mean dates (nearest day and standard deviation) of initiation of the 20 first and second clutches were 30
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May (SD 2.9 days) and 30 June (SD 3.2 days), respec- tively, and the mean number of days between initia- tion of first and second clutches was 30.2 days (SD 2.3 days). Mean initiation of first clutches by females with double broods followed the earliest dates that clutches were initiated in the population within | day (1975), 3-9 days (1976), 0-2 days (1984), 0-3 days (1985), and 1-3 days (1986). Initiation of second clutches preceded the last dates of the season for fe- males still attempting to lay clutches by 6 days (1975), 0-7 days (1976), 3—7 days (1984), 7-11 days (1985), and 1-14 days (1986). The mean number of days be- tween dates of fledging of the last nestling from first broods and dates of clutch initiation at unparasitized second nests (7 = 16 nests) was 3.6 days (SD 1.5 days): 2 days (n = 2 nests), 3 days (7 nests), 4 days (4 nests), 5 days (1 nests), 6 days (1 nest), and 8 days (1 nest).
Parasitized nests were excluded from this analysis because of possible interference with initiation of the Yellow Warblers’ clutches; indeed, a delay of 3 days in the completion of the clutch occurred at one nest par- asitized in 1986 (Table 1), in which the Yellow Warbler buried the eggs. This nest eventually failed (see Clark and Robertson (1981) and Guigueno and Sealy (2010) for details of the chronology of laying by Yellow War- blers parasitized by Brown-headed Cowbirds).
Discussion Documentation of double brooding
Data presented in Table | provide the first published evidence that Yellow Warblers attempt second broods in some years. Double brooding by Yellow Warblers has not been confirmed elsewhere in North America (but see below), but it has been confirmed in a non- migratory population on the Galapagos Islands, Ecua- dor (Snow 1966), located at the equator. Snow record- ed a single marked pair that attempted to rear two broods in each of two consecutive years, but in both years the second attempt failed. He added (Snow 1966, page 46) that the “season is amply long enough for [rearing second broods], and two broods are probably common.” The fact that double brooding has not been recorded at other sites, tropical or temperate, probably reflects the lack of observations of uniquely marked individuals throughout the breeding season.
These data support an earlier observation of an un- marked pair of Yellow Warblers that suggested dou- ble brooding in Manitoba, along the west shore of Lake Winnipeg, in 1978 (Bancroft 1979; also see Gollop 1979). Dates of initiation of the first and second clutch- es were in line with those presented for Delta Marsh and Lake Manitoba in Table |. This pair’s first nest was under construction on 26 May when it was first observed, and by 2 June it contained two Yellow War- bler eggs. An undetermined number of young had left the nest by 23 June, but by 7 July, the (same?) female was incubating 3 more eggs in the same nest from
SEALY: DOUBLE BROODING BY YELLOW WARBLERS AT DELTA MARSH, MANITOBA 47
which the first brood had fledged. Again, an undeter- mined number of young, in the second brood, fledged by 27 July, as noted by feces on foliage near the empty nest and audible vocalizations of fledglings and adults in a nearby hedge (Bancroft 1979), Both adults fed young from the first brood, but it was not reported whether both cared for young in the second brood.
Post-hoc examination of the nest by H. W. R. Cop- land of the Manitoba Museum in Winnipeg after the second brood had fledged revealed the nest had been parasitized by a Brown-headed Cowbird during the laying of the second clutch, whereupon the Yellow War- bler buried the Brown-headed Cowbird egg plus two of her own eggs, one of which was broken, under a new nest, and started again. The time spent burying the Brown-headed Cowbird egg and her own eggs, recon- structing the nest, and replacing the initial eggs of the second clutch suggests the final clutch was initiated on 28 or 29 June, consistent with the dates of initiation of second clutches at Delta Marsh, including the nest par- asitized in 1986 in which the Yellow Warbler buried the Brown-headed Cowbird and her first two eggs (Table 1).
Additional irrefutable records of double brooding by Yellow Warblers came to light during the review of this manuscript. One is in a population nesting at the north- ern limit of the species’ range, near Inuvik, Northwest Territories (68°21'N, 133°45'W), and the other is near Revelstoke, British Columbia (50°57'N, 118°10'W) (Anna Drake, personal communication). Near Revel- stoke, four cases of double brooding were recorded over eight years at a latitude similar to that of Delta Marsh. In 2004, a second-year female paired with an after-hatch-year male initiated first and second clutch- es on 25 May and 23 June, respectively. Three young fledged from each clutch. In 2005, two cases involved after-second-year females (one the female with the double brood in 2004 paired with the same male), which initiated first clutches on 27 and 30 May (fledg- ing 5 and 3 young, respectively), and second clutches on 24 and 28 June, respectively (fledging 3 young from each nest). In 2011, an after-second-year female pro- duced a maximum of three fledglings in the first clutch (initiated 30 May) and she produced a second clutch (date of initiation unknown). Dates of initiation of first and second clutches in this population were a few days earlier than those recorded at Delta Marsh (Table 1).
At Inuvik, Drake recorded a marked pair of after- hatch-year individuals that reared two broods in 2010, although the male was not observed while the female tended the second brood. First and second clutches were initiated on | June and | or 2 July, respectively, and the young fledged on 26 or 27 June and 23 or 24 July, respectively. These dates of initiation were re- markably similar to those recorded for first and sec- ond clutches at Delta Marsh (Table 1). Of the two cases at Delta Marsh in which first clutches also were initi-
48 THE CANADIAN FIELD-NATURALIST
ated on | June (both in 1984) (Table 1), the second clutches were initiated on 30 June, one or two days ear- lier than those at Inuvik.
Initiation of the earliest clutches by Yellow Warblers in other populations nesting at the northern limit of the range—Churchill, Manitoba (Briskie 1995), Yukon (Sinclair e¢ al. 2003), and Alaska (Kessel 1989)—has not been recorded before the middle of June. Briskie (1995, page 539), commenting on the length of the breeding season of the Yellow Warbler at Churchill, observed some clutches that were replaced after fail- ure early in the season, but found “... no evidence of double-brooding and [stated that] it is unlikely to occur. In the average year, even the earliest nests do not fledge young before late July and any second brood would require birds to remain in the area well past the end of the short subarctic summer.” The dynamics of breed- ing of this and other species at the northern limit of their range require additional study, especially when temperatures are increasing.
Implications of double brooding
The proportion of pairs with double broods recorded in the population in suitable years at Delta Marsh is not known but its determination was likely influenced, in the first instance, by the availability of marked pairs and, more importantly, by the number of marked indi- viduals whose first nests managed to survive through fledging, where ~60% of all nesting attempts by Yellow Warblers are depredated or fail due to inclement weath- er (Goossen and Sealy 1982; Guigueno and Sealy 2010). Probably no more than 5—10% of pairs attempt- ed to rear second broods in the 5 years in which they were recorded, but double brooding also may have occurred in 4 additional years of the study (1978, 1980— 82, see table III in Sealy 1995) that experienced similar nesting phenology. Nests tended by the marked pairs in those years may have failed before second clutches could be initiated, although if double brooding occurred, I should have recorded re-use of some first nests by unmarked pairs. Spring temperatures in 1979 and 1983 were lower and first clutches were not laid until 9 and 12 June, respectively (table III in Sealy 1995), proba- bly too late for double brooding.
Within the liniits of the small sample size of Yellow Warbler nests parasitized by Brown-headed Cowbirds (all of them second nests) (Table 1), it is noteworthy that parasitism was rejected at one of the four nests. Females tend to bury Brown-headed Cowbird eggs in the latter portion of the clutch-initiation season, but almost all females accept Brown-headed Cowbird eggs towards the end of the breeding season, when they are running out of time (Clark and Robertson 1981; Sealy 1995; Guigueno and Sealy 2010). This single instance of burial was unusual because it was initiated only two or three days before the last Yellow Warbler eggs of the season were laid at Delta Marsh in 1986 (table III in Sealy 1995).
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Short-lived individuals (Klimkiewicz ef al. 1983) might be expected to raise more than one brood in years when conditions are favourable (Evans Ogden and Stutchbury 1996), but they would have to be res- ponsive to early spring temperatures. In a study of arrival and clutch initiation by Yellow Warblers over 30 years at Delta Marsh, Mazerolle er al. (2011) report- ed that individuals exhibited considerable plasticity in the dates of clutch initiation in response to mean May temperatures. This plasticity was observed only at the beginning of the breeding season, as Yellow Warblers molt and migrate early (Morton 1976) and arrive on the wintering grounds from Mexico south to Peru where they compete for feeding territories, as early as late August (Neudorf and Tarof 1998). Rigid scheduling of molt and migration may preclude attempts to rear second broods, except in early seasons, but this may become more frequent with increasing temperatures.
Acknowledgements
I thank J. Briskie, D. Busby, H. den Haan, J. Goos- sen, K. Hobson, D. MacKenzie, R. Olenick, G. (Bier- mann) Pohajdak, J. Porter, and G. Sutherland for assis- tance in the field during the early years of the research on songbirds at Delta Marsh, Manitoba, which includ- ed considerable assistance with banding and colour- marking. I thank an anonymous reviewer and Anna Drake for constructive comments offered during the review of the manuscript. In addition, I would like to thank Anna for allowing me to include the record of double brooding by a pair of Yellow Warblers at an even more northerly latitude and D. J. Green, M. Hepp, and S. P. Quinlan for providing data from a site near Revelstoke, British Columbia. This work was funded chiefly by the Natural Sciences and Engineering Re- search Council of Canada, augmented by substantial in-kind support provided by the Delta Marsh Field Station (University of Manitoba).
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Received 6 June 2013 Accepted 8 July 2013
Asynchronous Breeding and Variable Embryonic Development Period in the Threatened Northern Leopard Frog (Lithobates pipiens) in the Cypress Hills, Alberta, Canada: Conservation and Management Implications
. Z LEA A. RANDALL!:3, LYNNE D. CHALMERS!:2, AXEL MOEHRENSCHLAGER!2, and ANTHONY P. RUSSELL
‘Centre for Conservation Research, Calgary Zoological Society, 1300 Zoo Road NE, Calgary, Alberta T2E 7V6 Canada Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, Alberta T2N 1N4 Canada 3Corresponding author: lear@calgaryzoo.com
Randall, Lea A., Lynne D. Chalmers, Axel Moehrenschlager, and Anthony P. Russell. 2014. Asynchronous breeding and
variable embryonic development period in the threatened Northern Leopard Frog (Lithobates pipiens) in the Cypress
Hills, Alberta, Canada: conservation and management implications. Canadian Field-Naturalist 128(1): 50—S6. Understanding breeding phenology is critical for establishing monitoring strategies, comprehending population dynamics, and developing conservation actions for at-risk species, such as the Northern Leopard Frog (Lithobates pipiens). The timing of spawning and hatching in the Northern Leopard Frog may be highly variable depending on regional environmental condi- tions, which can make establishing the timing of surveys difficult. In spring 2006, eggs were laid over 30 days (24 April to 23 May) and hatching occurred over 2 weeks (14-28 May) at three neighbouring ponds in Cypress Hills, Alberta, Canada. Although spawning occurred over a month, all eggs hatched within a 2-week period, indicating variable embryo development rate. Among 26 egg masses, eggs laid later in the season developed approximately four times faster than those laid earlier, and Akaike information criterion-ranked models suggested that both Julian date and water temperature were important predictors of embryo development rate: later spawning date and warmer water were associated with faster rates. Some egg masses survived colder temperatures than previously reported for this species. Asynchronous breeding and variable development rates reveal the need to conduct multiple surveys over the breeding season, even within a small geographic area, to document reliably the presence of egg masses and identify breeding habitat. Identification of key breeding habitat is necessary to mitigate human-caused disturbances of such regionally imperiled species.
Key Words: Northern Leopard Frog; Lithobates pipiens; amphibian; breeding; egg; conservation; embryo development: spawn- ing period; phenology; Cypress Hills; Alberta
Introduction its range in the 1970s and 80s (Roberts 1981*; Leonard
Breeding phenology and the time between spawning et a/. 1999), perhaps due to such factors as disease, and hatching may be highly variable within and among drought, competition by invasive species, and habitat populations of amphibians (Thumm and Mahony 2002; _ loss and fragmentation (COSEWIC 2009*). As a result, Ryan and Plague 2004) as a result of an assortment of _ the western boreal—prairie populations of Northern exogenous and endogenous factors (Reading 1998; Leopard Frogs are designated of “special concern” by Oseen and Wassersug 2002; Grant et al. 2009). This | the Committee on the Status of Endangered Wildlife in variability can make timing of population surveys chal- Canada (COSEWIC 2009*) and “threatened” under lenging. Alberta’s Wildlife Act (AESRD 2012*).
Industrial development continues to increase in Al- We investigated predictors of spawning time and berta, particularly in association with oil and gas extrac- | embryo development rate of Northern Leopard Frogs, tion, and may negatively affect wildlife unless proper _ such as temperature and time of year, as part of a larger mitigation measures can be implemented. Permits for study of tadpole microhabitat selection and juvenile dis- industrial exploration and extraction often stipulate a _ persal behaviour. Natural history observations of this requirement for amphibian surveys before land devel- type may be useful for improving the probability of opment if at-risk amphibians are predicted to inhabit the detection by providing information regarding the timing area (Dr. David Prescott, Species at Risk Biologist, of the breeding period and the frequency of surveys Alberta Environment and Sustainable Resource Devel- required to identify and protect important habitat. opment, personal communication, 29 March 2012).
However, for these surveys to be effective, they must Study Area be carried out at a time and in a manner appropriate for Our study was conducted in and near Cypress Hills the species of interest. Interprovincial Park (49°39'N, 110°01'W) which strad-
Once widely distributed and abundant in North dles the border between Alberta and Saskatchewan and America, the Northern Leopard Frog (Lithobates pip- is just north of the Sweetgrass Hills of Montana (Fig- iens) disappeared from much of the western portion of ure 1). The Alberta portion of the Cypress Hills is char-
50
2014
Legend
@ Breeding Pond —— Road
Cypress Hills Interprovincial Park
RANDALL ET AL.: BREEDING AND EMBRYONIC DEVELOPMENT IN NORTHERN LEOPARD FroGs 5]
FiGure |. Locations of four Northern Leopard Frog (Lithobates pipiens) breeding ponds surveyed in 2006 in and near Cypress Hills Interprovincial Park, Alberta, Canada (49°39'N, 110°01'W).
acterized by grasslands and boreal forest. Elevation ranges from 1370 m to 1465 m, and average annual temperature is lower than that of the surrounding grass- land plains (Greenlee 1981*). These environmental conditions likely present challenges to the reproduc- tive success of Northern Leopard Frogs.
In 2006, we drove along roads and flew over the study area in a fixed-wing aircraft to identify potential Northern Leopard Frog breeding ponds within a 25-km radius of our main study pond (Pond 1, Figure 1). Al- though other breeding ponds may have been present, these four represented all known breeding ponds at the time.
Pond | was 0.1 ha in surface area and was surround- ed by Populus spp. woodlands on the east, west, and south sides; the north side had a relatively steeper slope of mixed grass prairie (Fraser 2007). Ponds 2 and 3 had surface areas of 0.17 ha and 0.04 ha, respectively, and were also surrounded by mixed grass prairie and aspen woodland. Pond 4 had a surface area of 0.24 ha and was surrounded by mixed forest, mainly white spruce (Picea glauca) on the west and north sides and dead- fall on the south and east sides.
Methods
Study organism . . Adult Northern Leopard Frogs are medium-sized frogs, 5-10 cm long from snout to vent (Hine et al.
1981*: Russell and Bauer 2000). Within a population, breeding period ranges from a few days to a few weeks (Wells 1977). In Alberta, spawning occurs over a short interval between late April and early June (Russell and Bauer 2000; Kendell 2002) at temperatures of 10—25°C, although spawning may be prolonged if the temperature drops below this range (Hine e¢ al. 1981*; Gilbert ez al. 1994; Kendell 2002*). Females deposit 600-7000 eggs in a single egg mass, which they attach to sub- merged vegetation. Preferred water bodies are ephemer- al or fishless permanent ponds or slow-moving back- waters of streams and rivers in shallow water (AESRD 2012*). The period from spawning to hatching may last from 5 days to 3 weeks (Russell and Bauer 2000; Werner et al. 2004) and metamorphosis typically occurs between July and August in Alberta (Kendell 2002*).
Observation techniques
Beginning approximately 30 minutes after sunset, we listened for breeding calls of adult male Northern Leopard Frogs for up to 20 minutes (AESRD 2013*). If calls were detected, we returned the following day to confirm spawning.
We conducted call and shoreline surveys from 25 April to 8 June 2006 and searched the shoreline of each pond at least once every 2 days for new egg masses to determine the duration of the breeding season and the embryo development period (Merrell 1977*; Dorcas et
Nn i)
al. 2010; Paton and Harris 2010). Individual egg mass- es were identified by differences in either their size or shape or the stage of development of the embryos (Mer- rell 1977*). Their location along the shoreline was marked with a flag to prevent counting an egg mass twice (Gilbert et al. 1994; Dougherty ef a/. 2005). During each survey, egg masses were identified as hatched or unhatched (egg mass intact). Hatching was confirmed when newly hatched tadpoles were seen ag- gregating around the egg mass, feeding on the remain- ing jelly.
For each egg mass, we measured its depth below the water surface, distance to adjacent masses, and distance from the shoreline using a metre stick. During shoreline surveys, we measured the temperature of the water within 10 cm of each egg mass using a Hanna pH pen thermometer. We considered the breeding season com- plete once male calling had ceased and no new egg masses had been observed for at least 2 weeks.
Statistical analysis
We ran a one-way ANOVA to determine whether ponds differed with respect to water temperature when egg masses were laid, followed by Tukey’s honest sig- nificant difference (HSD) test. We assessed whether residuals were normally distributed using a Shapiro— Wilk goodness-of-fit test (W > 0.93). We used Julian date (JD) in our models to account for seasonal vari-
150 j H j i =] 2 S SANQOSE WSN £ Sotte @ 130 ROleeTs s $3 ese 2°) HEBER g 1% HE res Se ee 338 110
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ation of environmental factors, such as photoperiod. To evaluate predictive factors related to embryo development, we first performed an exploratory regres- sion analysis of embryo development rate versus JD and water temperature (WT). To further investigate the relation of JD and WT to embryo development rate we used restricted maximum likelihood mixed-model regression (JMP, version 7, SAS Institute Inc., Cary, North Carolina, USA). Pond was a random factor; all other factors were fixed. We formulated a set of can- didate models that all included pond alone, pond with JD or WT, or pond with both JD and WT in an additive model and with the interaction of JD and WT. Because collinearity of predictor variables can yield unstable parameter estimates and inflated standard errors (Quinn and Keough 2002), we verified that JD and WT were not highly correlated (77 < 0.6) before we included them together in a model (Royston and Sauerbrei 2008). We compared models using small-sample-size Akaike information criterion (AIC_) to select the “best” model given a candidate set of models and considered models to have equivalent support if AAIC. was < 2 (Burnham and Anderson 2004). We assessed the goodness-of-fit of the global model using a Shapiro—Wilk test (W > 0.90).
Results Spawning occurred over 30 days at ponds 1-3, beginning on 24 April and ending 23 May (Figure 2).
May 29
May 22
May 15
May 08
May 01
Apr 24
Pond
euRE oD” : J eye are een ey Seat. : Ri: FIGURE 2. Development period for Northern Leopard Frog (Lithobates pipiens) eggs at ponds 1, 2, and 3
in Cypress Hills
Interprovincial Park, Alberta (see Figure 1) in April and May 2006. Each column of black circles represents days
from spawning to hatching for one of the 26 egg m
asses observed. The shaded area represents the period during
which egg masses were present at all three ponds (10-17 May).
2014 RANDALL ETAL.: BREEDING AND EMBRYONIC DEVELOPMENT IN NORTHERN LEOPARD FROGS 53
Although calling and spawning were confirmed at pond 4, we were unable to monitor egg masses because pollen blanketed more than half of the water surface, affecting our ability to observe them. Hatching occurred at the three remaining ponds over 2 weeks, beginning 14 May with the last eggs hatching on 28 May. We ob- served a total of 26 egg masses: 14 in pond 1, 7 in pond 2, and 5 in pond 3. Egg masses were laid within 2-10 cm of the water surface, typically grouped togeth- er in shallow areas within 2—3 m of the shoreline. All monitored egg masses survived to hatching, but we were unable to monitor the proportion of eggs that hatched successfully.
The onset of spawning differed by only 3 days be- tween ponds | and 2, but occurred approximately 2 weeks later at pond 3. The WT near each egg mass on the day of spawning was significantly higher at pond 3 (17.4°C + 1.9 [mean + standard error], = 0.40, F, ,. = 7.62, P = 0.0029) than at ponds | and 2, but did not differ between ponds | and 2 (9.1°C + 1.6 and 9.1°C +
Apr 24 May 01 25 ‘ '
20
15
10
Embryonic development period (days)
115 120 125
May 08
1.1, respectively). At ponds | and 2, egg laying first occurred on 24 and 27 April, respectively. Up to five egg masses were laid on the same day in ponds | and 2, and the spawning period lasted for almost a month. Egg masses were detected simultaneously at all three ponds during only | week, 10-17 May.
At the time eggs were laid WT ranged from 5.7°C to 25.8°C. At pond |, WT dipped as low as 3°C during egg development (27 April). Time from spawning to hatching ranged from 5 to 20 days and decreased with JD at laying (Figure 3). Eggs deposited at the beginning of the breeding season (24 April) took about four times as long to hatch as the last eggs laid (23 May).
Although we found a strong, negative relation be- tween embryonic development period and JD, the rela- tion between that period and spawning temperature was not as strong (Figure 4). The top model, with 93% of the AIC, weight, was an additive model that in- cluded WT and JD (Table 1). No other models were <2 AAIC, of the top model.
May 15 '
140
130 135 145
Julian date
FIGURE 3. Relation between dev (Lithobates pipiens) egg Masses The numbers above eac
elopment period and Julian date (24 April-28 May 2006) for 26 Northern Leopard Frog at ponds 1, 2, and 3 in Cypress Hills Interprovincial Park, Alberta (see Figure 1). h symbol represent the number of egg masses laid on that date. Symbols for ponds at which
egg masses were laid on the same date have been slightly offset (~ = 0.91).
54 THE CANADIAN FIELD-NATURALIST Vol. 128
25
A Pond 1
CO Pond 2 @ Pond3
20
15
10
Embryonic development period (days)
8 10 12 14 16 18
Water temperature (°C)
FIGURE 4. Relation between development period (24 April—28 May 2006) and spawning temperature for 26 Northern Leop- ard Frog (Lithobates pipiens) egg masses at ponds 1, 2, and 3 in Cypress Hills Interprovincial Park, Alberta (see Figure 1). Numbers above each symbol represent the number of egg masses laid at that water temperature. Symbols for ponds at which egg masses were laid at the same water temperature have been slightly offset (7? = 0.32).
TABLE 1. Variation in development period of Northern Leopard Frog (Lithobates pipiens) eggs with Julian date (JD) and water
temperature (WT). The top model was selected using Akaike information criterion adjusted for small sample size (AIC). 3.08 aVvYa—Naa@a@oQqoQqwo@maomamaSq_q_—_ aa —“—“_O—————————————————————————
Model —2LL K AIC, AAIC, AIC, weight Embryo development period = Pond + JD + WT ODESY 5) 115.59 0.00 0.93 Embryo development period = Pond + JD 111.24 d 121.14 5:55 0.06 Embryo development period = Pond + JD +WT + JD* WT 107.59 6 124.01 8.42 0.01 Embryo development period = Pond + WT 158.07 4 167.97 52.38 0.00 Embryo development period = Pond 164.85 3 171-95 56.36 0.00
Note: -2LL is —-2*model log-likelihood, K is the number of parameters in the model. AAIC. is the difference between the AIC, of each model and the top model.
Discussion Werner ef al. 2004). It is interesting to note that, where- The onset of spawning was not synchronous in our —_as spawning occurred over the course of a month. all study area and varied by over 3 weeks among our ponds. _ eggs hatched within a 2-week period with the first eggs However, spawning was often synchronous within a deposited taking almost four times as long to develop as pond, with several egg masses laid ona single day. The __ the last eggs laid. spawning period was also protracted, lasting up to 30 Eggs were laid at WT ranging from 5.7°C to 25.8°C. days at a single breeding pond (pond 1). The duration which is consistent with known egg temperature tol- of the breeding season and the embryonic development __erances for this species (Moore 1939, 1949). However. period was consistent with other published reports our minimum spawning temperature was more than (Merrell 1968; Wells 1977; Russell and Bauer 2000; 2°C colder than that recorded for Northern Leopard
2014 RANDALL £7 4L.: BREEDING AND EMBRYONIC DEVELOPMENT IN NORTHERN LEOPARD FROGS
Erogs in Quebec, which do not spawn at WT below 8°C (Gilbert et al. 1994). In addition, WT at one of our ponds dropped to 3°C during the development period, which is 2°C below the reported threshold for normal embryonic development in this species (Moore 1949). However, the temperature at the centre of an egg mass can be up to 2°C warmer than the surrounding water (Hassinger 1970). Although the four affected egg mass- es survived to hatching, we were unable to evaluate whether the embryos had developed normally.
The top model for embryonic development period included both JD and WT as predictive variables, sug- gesting that temperature alone is not sufficient to explain differences in development period, which might also be affected by seasonal differences in the region. However, there was no evidence that the effect of tem- perature on development changed over time (the inter- active model was > 8 AAIC, from the top model). Al- though it has long been known that the development of Northern Leopard Frogs is temperature dependant (Atlas 1935: Moore 1939), clearly this is not the only factor affecting embryo development period.
Conservation and Management Implications Industrial development permits issued by regulators often stipulate that developers determine whether at- risk species, such as the Northern Leopard Frog, are present and establish appropriate mitigation strategies to reduce or eliminate negative impacts of their activ- ities. Often only single surveys are conducted to deter- mine the presence or absence of at-risk amphibians (Kendell 2003*). Our results suggest that inappropri- ately timed breeding surveys may fail to detect North- ern Leopard Frogs and could, thus, limit the ability to develop appropriate strategies to conserve this species. Even within our small study area, egg masses would have been observed in all three ponds during only | week — a narrow timeframe for the completion of ef- fective and comprehensive egg-mass surveys. Because breeding phenology is likely to vary annually, region- ally, and locally, we recommend that researchers adjust the timing of their surveys so that they are relevant to each specific site. To identify breeding ponds, multiple breeding surveys separated in time should be conduct- ed. The need to adjust the timing and number of sur- veys necessary to identify breeding sites is not unique to Northern Leopard Frogs (AESRD 2013*). As such, we recommend that breeding phenology be considered when developing monitoring strategies or industrial mitigation procedures for amphibians elsewhere.
Acknowledgements . . . . All research was conducted in compliance with Uni-
versity of Calgary Animal Care Protocol BI 2005-39 and the Calgary Zoo BRRC 2005-05 approval number. We are grateful for funding provided by Husky Energy and Cenovus Energy Ltd. We thank Typhenn Brichieri- Colombi for providing the map of the study area.
Nn Nn
Documents Cited (marked * in text)
AESRD (Alberta Environment and Sustainable Resource Development). 2012. Alberta Northern Leopard Frog recovery plan, 2010-2015. AESRD, Edmonton, Alberta. Page 34.
AESRD (Alberta Environment and Sustainable Resource Development). 2013. Sensitive species inventory guide- lines. AESRD, Edmonton, Alberta. Page 128.
COSEWIC (Committee on the Status of Endangered Wildlife in Canada). 2009. COSEWIC assessment and update status report on the Northern Leopard Frog Litho- bates pipiens, Rocky Mountain population, Western Bore- al/Prairie populations, Eastern populations in Canada. COSEWIC, Ottawa, Ontario. 69 pages.
Greenlee, G. M. 1981. Soil survey of Cypress Hills, Alberta, and interpretation for recreational use. Alberta Research Council, Edmonton, Alberta. 77 pages.
Hine, R. L., B. L. Les, and B. F. Hellmich. 1981. Leopard