A Skeletochronological Study of the Age Structure, Growth, and Longevity of the Mountain Yellow-Legged Frog, Rana Muscosa, in the Sierra Nevada, California

Copeia, 2007(4), pp. 986–993

A Skeletochronological Study of the Age Structure, Growth, and Longevity of the Mountain Yellow-legged Frog, Rana muscosa, in the Sierra Nevada, California

KATHLEEN R. MATTHEWS AND CLAUDE MIAUD

We used skeletochronology to determine the ages of 149 (74 females, 44 males, and 31 juveniles) Mountain Yellow-legged Frogs (Rana muscosa) from 13 locations (elevation 1509–3501 m) throughout their current range in the Sierra Nevada mountains of California. Lines of arrested growth (LAGs) from excised toe bones were distinct in these high elevation frogs, and each LAG was assumed to represent one year of age. Females ranged in age from 0–10 years (mean = 4.1 years) and males from 0–8 years (mean = 4.0 years). The skeletochronological age was that of the post- metamorphic frog and did not include the tadpole stage. Mountain Yellow-legged Frogs spend 3–4 years as tadpoles, but no age markers are found in their cartilaginous skeletons; thus, their total age, if both tadpole and post-metamorphic stages were included, would range up to 14 years. Females were significantly longer (snout–vent length: SVL) than males and had greater mean mass, but there was no difference in the mean ages. Juvenile frogs of unknown sex ranged in age from 0–3. The von Bertalanffy growth curve demonstrated that female SVLs were larger than males for all ages. Using a semi-parametric growth model, we also found that elevation within the Sierra Nevada range was an important variable in the relationship between SVL and age; frogs from lower elevation sites were consistently larger at a given age when compared to higher elevation sites. For each increase of 1000 m in elevation, the estimated length (on average) decreases by 8.7 mm. This is the first age determination study of a Sierra Nevada amphibian, and compared to other anuran species, Mountain Yellow-legged Frogs were found to be relatively long-lived, which will have implications for restoration and recovery plans.

HE Mountain Yellow-legged Frog, Rana response of amphibians cause the formation of T muscosa, is endemic to the Sierra Nevada bone growth marks, including zones of thicker mountain range of California and was historically layers of bone laid down during periods of fast a common inhabitant of lakes and ponds at osteogenesis, and lines of arrested growth 1400–3700 m (Grinnell and Storer, 1924). De- (LAGs) formed during periods when osteogen- spite the fact that its habitat is protected within esis is slow or inactive (Castanet and Smirina, national park and national forest wilderness 1990). A zone followed by a LAG typically areas, R. muscosa is now extirpated from more corresponds to a one-year cycle of activity in cold than 50% of its historic localities (Drost and or temperate regions and has been confirmed as Fellers, 1996; Jennings, 1996). It was recently an annual mark for several amphibians (Smirina, found warranted but precluded for federal 1994). Endangered Species Act protection (U.S. Fish Due to the extreme environment encountered and Wildlife Service, 2003). Restoration and at high elevations (e.g., long winters, sustained recovery plans and viability models will require freezing, and low temperatures), R. muscosa are a better understanding of the demography of R. only active for a few months during the summer muscosa, including information on the age after snowmelt and before the winter freeze structure and longevity of this frog. Little is (Pope and Matthews, 2001). High elevation known regarding the lifespan or age structure of amphibian growth is punctuated because the any Sierra Nevada amphibian. active season is short, thus skeletochronology Skeletochronology is an effective tool and has should be effective for high elevation species like been widely used for over 20 years to evaluate age R. muscosa. The method has been effectively used and growth in amphibians (Castanet and Smir- to determine ages of many ranids (Leclair and ina, 1990; Smirina, 1994; Esteban et al., 1996). Castanet, 1987; Leclair et al., 2000; Tsiora and Annual seasonal changes and the physiological Kyriakopoulou-Sklavounou, 2002), including

# 2007 by the American Society of Ichthyologists and Herpetologists MATTHEWS AND MIAUD—RANA MUSCOSA AGE AND GROWTH 987 high elevation species (Miaud et al., 1999; slides and stained with hematoxylin. The Reaser, 2000), but has not been applied to any slides were coverslipped using a toluene-based Sierra Nevada amphibians. This technique re- resin, creating a permanent mount. Magnifica- quires collection of a long bone, such as a toe, to tions of 100–2503 were used to examine the toe be analyzed for LAGs. sections. The objective of this study was to use skeleto- Assumptions in the standardized analysis for R. chronology (toe bones) for age determination in muscosa were that LAGs form during winter when R. muscosa. By sampling frogs of all sizes activity is reduced, and the first LAG is formed throughout the current range in the Sierra during the first winter of life after metamorpho- Nevada, we also investigated how specific vari- sis (Leclair and Castanet, 1987). There is no LAG ables such as sex and elevation are related to deposition during the aquatic tadpole phase their growth or longevity. because the skeleton is cartilaginous and younger tadpoles lack limbs. The absence of LAGs in three-year-old American Bullfrog tadpoles has MATERIALS AND METHODS been reported (Khonsue and Matsui, 2001). To estimate ages of R. muscosa, toes were Thus, the skeletochronological age is that of collected from frogs at 13 study sites throughout the adult frog and does not include the tadpole theSierraNevada(Fig.1).Eachfrogwas stage. Rana muscosa tadpoles overwinter for at measured for snout–vent length (SVL) in mm least two to three years (Zwiefel, 1955; Cory, using calipers, mass (g) was recorded using 1963; Bradford et al., 1993), up to four years at Pesola spring scales, and each frog was sexed higher elevations (Matthews, pers. obs.), and (adult male, adult female, or juvenile). Sex was metamorphosis typically occurs in late summer. determined by the enlarged nuptial pad at the At lower elevations metamorphosis may occur base of the inner-most finger found on males. If after 1–2 years as a tadpole (Storer, 1925). a frog was greater than 40 mm (SVL) and had no In amphibians, inner bone layers and LAGs nuptial pad, it was categorized as a female. Frogs may be lost (endosteal resorption) in older less than 40 mm SVL could not be sexed and animals (Smirina, 1994). Uncertainty about the were categorized as juveniles. A portion of the number of years of growth resorbed is a source of 4th digit on the right hindlimb was removed, and age analysis error. Because the season of most the frog was then released. We excised bones by rapid growth of the adult frog is shortest during cutting at a point that left the two most distal the year of metamorphosis, the bone formed in phalanges and their two associated joints com- the summer/fall of the year of metamorphosis pletely intact. The sample was placed in a labeled (located internal to the first LAG) is thinner than envelope for later lab processing; no special bone of the following year. Because the bone storing of the bone was required. The segment of layer of the first year is thinnest, it is the most the phalanx that is suitable for aging by counting likely to be resorbed in older frogs. In the oldest annual layers was very short. Closer to the frogs, more than one bone layer may be absent. epiphyses, the thinner-walled and younger bone We attempted to identify the first layer present by lacked the annuli formed earlier in life. Very using these criteria: 1) thickness of the layer in near the epiphyses, the phalanx is mostly question; 2) thickness of the layer external to it; cartilage and entirely lacking in annuli. The and 3) presence of proximal (3rd section of specific bone section used for age determination phalanx) peripheral bone. The exact time of year was the second, most distal phalanx, and it was at which bone growth resumes is not well known. important to include the joints between the 1st The best method for locating the first LAG is to (distal) and the 3rd (proximal) phalanx in each observe the bones of recently metamorphosed sampled toe bone. The sectioning point was then frogs. In these bones, the first LAG without selected to begin just proximal to the midpoint. resorption is identifiable. By measuring the A series of six sections were taken at intervals that distance of the first LAG from the center of the extended distally. medullar cavity, comparison with bones of larger The toes were prepared for sectioning by frogs can determine whether the first and isolating the second phalanx and measuring the subsequent LAGs are eroded. For the purpose width of this bone to the nearest 0.25 mm. The of age analysis, we assumed that the peripheral bone was then decalcified and embedded in layer of bone that was formed by July would a paraffin block (Leclair and Castanet, 1987). represent only a part of the annual increment Six 14-micron sections were made on a rotary and would be very thin, particularly in older microtome at intervals calculated to include frogs. For example, a frog determined to have a section at the exact mid-diaphysis of the bone. eight LAGs (Fig. 2) includes seven identifiable The sections were mounted onto microscope LAGs and one resorption area. 988 COPEIA, 2007, NO. 4

Fig. 1. Map of sites throughout the Sierra Nevada where Rana muscosa toes were sampled.

It was assumed that the number of LAGs is assumed to be within about ten microns of the reflected chronological age of the metamor- medulla of the bone and is likely to be partially phosed frogs (juveniles and adults). All toe or totally resorbed in animals older than one samples were processed, and LAGs were counted year. Total age was estimated by adding 3–4 years by a commercial laboratory (Matson’s Laborato- of tadpole life to LAG counts. ry, Milltown, MT) after an initial consultation We tried to sample frog toes from representa- with Gary Matson to identify LAGs and ensure tive areas reflecting the current distribution from agreement on age estimates. After we received the northern Sierra Nevada (Plumas National the mounted slide samples, we also confirmed Forest) to Kings Canyon National Park in the age estimates. Ages were estimated by counting south (Fig. 1), and also from a range of eleva- the first identifiable line of arrested growth tions. To minimize damage to small populations, (LAG) that was preceded by a well-developed we restricted our sampling to areas that had layer of bone. The LAG of the first winter of life more than 15 adults. We attempted to sample MATTHEWS AND MIAUD—RANA MUSCOSA AGE AND GROWTH 989

though November–December (Matthews, unpubl. data). Some frogs at the lower elevation were also found in streams while higher elevation frogs were typically in lakes and ponds. To explore the relationship between age and length (SVL), we started by fitting the widely used von Bertalanffy (von Bertalanffy, 1938) function describing SVL as a function of age. The von Bertalanffy growth function is used extensively in fisheries research and has now been used in several amphibian growth studies (Miaud et al., 2000; Cogalniceanu and Miaud, 2003):

Model ½1 LtðÞ~Lmax{ðÞLmax{Lmin exp½{KtðÞ{t0 ,

Fig. 2. Photograph of toe cross section showing where t 5 age (an integer of the number of eight lines of arrested growth (LAGs) for Rana LAGs), L (t) 5 SVL at time sampled (age t), t0 5 muscosa. Scale bar 5 25 mm. offset to 0.5 years old to account for not sampling true age 0, Lmax 5 maximum SVL, SVL of frog for a representative size range of those juveniles and infinite age, Lmin 5 SVL at one year old, K5 growth adults available at each site. We also sampled rate (specifically the von Bertalanffy growth co- small frogs (,40 mm; n 5 9) at site 11 (Dusy efficient) or the rate at which growth reaches Lmax. Basin) to help identify the first LAG; these Differences in growth coefficients and Lmax were juvenile frogs were not included in any analyses. compared using t-tests. We fit equation/model [1] We were unable to find adequate numbers of to data from all sites, but separately for males and frogs in the central Sierra near Lake Tahoe, or females; juvenile frogs were not included. south of Kings Canyon National Park in Sequoia Because the growth curves may be different National Forest. In these areas, frog abundance among the 13 sites due to elevation, we also fitted has declined to such an extent that sampling was a semi-parametric regression model (model 2, deemed inappropriate. Because of the limita- Hastie et al., 2001) to determine whether tions in finding frogs, we were not able to elevation was affecting size at a given age. For randomly sample and instead tried to stratify example, frogs at lower elevations might be larger the sample throughout areas of the Sierra due to a longer summer activity period (typically Nevada where frogs are currently found. from May–November) during the year cycle. In the From July 2001 through August 2003, we Sierra Nevada the lowest elevations where R. sampled 162 frog toes from 13 locations (num- muscosa are currently found include the northern ber of samples per site ranged from 3–19) in the and western sites (Fig. 1). In contrast to the von Sierra Nevada (Fig. 1) from Lone Rock Creek, Bertalanffy growth model, this model did not Plumas National Forest in the north assume any specific shape for the growth curve. (40u11927.60N, 120u37916.20W) to Sixty Lakes The shape of the growth curve was estimated from Basin, Kings Canyon National Park in the south the data using cubic spline functions: (36u48917.80N, 118u2593.10W). Elevations ranged from 1509 m at Lone Rock Creek to 3501 m at Model ½2 L ~ sex z sage,sexðÞz elevation Upper Mills Lake in the Sierra National Forest. z error, The distance between sites 1–13 was 422 km. The section of the Sierra Nevada between sites 1–2 where L 5 SVL of R. muscosa,sex5 a categorical and 3–4 did not have adequate populations of variables with 3 levels (female, male, juvenile), age adult frogs. 5 estimated age using LAGs, elevation 5 elevation Similar to other amphibians, R. muscosa have of the site where the frog was captured, error 5 shorter activity periods as elevation increases independent random error terms, s ( ) 5 spline (Morrison and Hero, 2003). Frogs at higher function describing the nonlinear relationships elevation sites (.3000 m) typically are active between the explanatory variables and the re- from post-snowmelt (varies year to year from sponse L. This model was then used to determine June–late July) until the lakes freeze (late if there were differences in male and female SVL at October–December). In contrast, frogs at lower a given age and if there were differences in SVL at elevation (,2000 m) in the northern Sierra age throughout the sampling area. These analyses Nevada have considerably longer activity and were done only using male and female data (no growth periods and can be active from April–May juveniles). 990 COPEIA, 2007, NO. 4

TABLE 1. SUMMARY OF SVL, MASS, AND LAGS (AGES) OF MOUNTAIN YELLOW-LEGGED FROGS SAMPLED IN THE SIERRA NEVADA.

SVL (mm) Mass (g) #LAGs (age)

Females min 40 7 0 n 5 74 max 87 76 10 mean 6 S.E. 63.6 6 1.3 32.5 6 1.9 4.1 6 0.3 Males min 42 8 0 n 5 44 max 68 40 8 mean 6 S.E. 56.1 6 1.0 21.3 6 1.2 4.0 6 0.3 Juveniles min 20 1.5 0 n 5 31 max 40 7 3 mean 31.6 6 0.8 3.8 6 0.3 0.9 6 0.1

RESULTS The von Bertalanffy growth curve (Fig. 3) demonstrates the differences between SVLs for From the 162 frogs sampled, a total of 149 (74 males and females at all ages, but showed great females, 44 males, and 31 juveniles) were aged; variability at each age. Female SVLs were larger the remaining were damaged or had inadequate than males for all ages. Females had larger Lmax bone sections that did not allow for proper than males (69.0 mm vs. 59.9 mm, t-test: P , analysis. Females ranged in age from zero (no 0.001). The growth coefficients (K) were not LAG) to ten years and had a mean age of 4.1 significantly different between males and females (Table 1). Males ranged in age from 0–8 years (K 5 0.50 6 0.30 for females, 0.41 6 0.3 for and had a mean age of 4.0. The number of males, males; t-test: P 5 0.10). females, and juveniles in each age group are Because of the considerable variation in size at found in Table 2. When estimated tadpole years a given age (Fig. 3), we explored the possibility (3–4 yr) are added, longevity extended to 13– that elevation may influence growth, and the 14 years in females and 11–12 years in males. semi-parametric regression model 2 indicated The females were larger than males at all ages that elevation was important in accounting for (Fig. 3). Females were significantly longer than some of the variation between observed and males (mean SVL 5 63.6 vs. 56.1, t-test: P , fitted SVLs (adjusted R2 5 0.78, non-parametric 5 0.001, df 116) and had greater mean mass than regression;Fig.4;model2P-values: Psex , males (32.5 g vs. 21.3 g, t-test: P , 0.001, df 5 0.0001, Ps(age,sex) , 0.0001, Pelevation , 0.0001). 116), but there was no difference in the mean ages (t-test: P 5 0.882). Juvenile frogs of unknown sex ranged in SVL from 20–40 mm, in mass from 1.5–7 g, and in age from 0–3 (Table 1).

TABLE 2. SUMMARY OF THE NUMBER OF MALES,FEMALES, AND JUVENILES IN EACH AGE CATEGORY.

Age Male Female Juvenile Total

0121013 1 3 12 16 31 277317 3108220 4 4 12 0 16 5 5 11 0 16 6 9 10 0 19 747011 81405Fig. 3. Fitted growth curves using model 1 (von 90000Bertalanffy growth model) with length (SVL) and 10 0 1 0 1 age data for male and female frogs. Ages do not Total 44 74 31 149 include tadpole phase. We offset t0 5 0.5 years to account for not sampling true age 0. MATTHEWS AND MIAUD—RANA MUSCOSA AGE AND GROWTH 991

up to five years for males. In lower elevation areas, Cogalniceanu and Miaud (2003) reported ages of 4–10 years for individuals in the R. esculenta complex from the Danube River flood- plains. Skeletochronology was also successful for determining ages of Wood Frogs (R. sylvatica); ages up to five years were reported from Quebec (Bastien and Leclair, 1992). Like most anurans, R. muscosa are sexually dimorphic (Monnet and Cherry, 2002); R. muscosa females were larger than males, similar to that seen in other ranid species (Reaser, 2000; Monnet and Cherry, 2002). From our studies in Kings Canyon National Park we knew that female R. muscosa were typically larger (SVL: mean 5 63.5 mm for females, mean 5 55.9 mm for males, n 5 1250 frogs, Matthews, unpubl. data) and heavier than males. The smaller sizes of males and possible higher vulnerability to predation may contribute to their shorter lifespan, although more data are needed to confirm. Only one frog was determined to be ten years (3501 m), Fig. 4. Observed versus fitted lengths (SVL) using the semi-parametric regression with elevation and no nine-year-old frogs were found, suggesting (model 2). Median absolute deviation is 5.0 mm. that survival to the older ages is rare. However, in Adjusted R2 for model 2 is 0.78. 2006 we caught 44 frogs (24 females and 20 males) of the 356 adult frogs originally tagged with PIT We found a mean average deviation of 5 mm tags in Dusy Basin, Kings Canyon National Park in between the observed and fitted values. The 1997 (Matthews, unpubl. data); these frogs were at slope of the elevation 520.0087 (S.E. 5 least ten years old (total age 12–13 years). 0.0012); for each increase of 1000 m in elevation, Although males of other species often are more the estimated length (on average) decreases by conspicuous and prone to predation when groups 8.7 mm. The scatter plot (Fig. 5) shows the of males aggregate and form large chorusing relationship between elevation and SVL; SVL groups during breeding (Shirose et al., 1993; decreases as elevation increases. This was a pat- Tsiora and Kyriakopoulou-Sklavounou, 2002), tern across sampling sites for both males and male R. muscosa lack vocal sacs (Stebbins, 2003), females to be larger at a given age at lower do not call during breeding, and do not form elevation sites. On average males were between breeding aggregations. Garter snakes and intro- 7.2–12.7 (95% CL) mm smaller than females. duced trout are common amphibian predators throughout the Sierra Nevada (Jennings et al., 1992; Matthews et al., 2002) and may target males DISCUSSION because of their smaller size. This is the first study using skeletochronology At lower elevations growth was faster and frogs to estimate the ages of a Sierra Nevada amphib- were bigger at most ages. This difference is likely ian. Because R. muscosa spend an extended due to the longer summer; at sites in the number of years as tadpoles (3–4 years), total northern Sierra Nevada (elevation 1509– age, including both tadpole and adult stages, 1872 m) frogs are active from April/May through ranged up to 14 years. Compared to other high November. In contrast, lakes and water bodies at elevation amphibians, R. muscosa is long-lived. higher elevations (.2500 m) are frozen or Although no age determination techniques were covered in snow for longer periods and keep used, Sherman and Morton (1993) estimated frogs snowbound for extended periods; thus, from tag recoveries that some female Bufo canorus they have a shorter active period, typically from were at least 15 years old from field sites near late June through early October (Matthews and Tioga Pass in the central Sierra Nevada Pope, 1999; Pope and Matthews, 2001). These (,3000 m). Reaser (2000) used skeletochronol- shorter active periods reduce feeding times, ogy to determine age of post-metamorphic R. resulting in reduced growth rates. luteiventris from the Toiyabe range in Nevada Skeletochronology was effective in age de- (elevations 2200–2700 m) and estimated that termination of R. muscosa. Mountain Yellow- ages ranged up to seven years for females and legged Frogs are relatively long-lived anurans, 992 COPEIA, 2007, NO. 4

Fig. 5. Elevation versus observed SVL (mm) for male (+) and female (&) frogs. Lines through the points were made with a scatterplot smoother of estimated lengths using model 2. and those at lower elevations were larger at a given understanding because of the frog’s status as age. This study demonstrated the need to sample a species of special concern. In Yosemite and across the frog’s current distribution as there were Sequoia–Kings Canyon National Parks, frog toe considerable differences in age and growth collections were permitted by the National Park throughout the Sierra Nevada. Because of their Service (Matthews YOSE 0037 and SEKI 041). age distribution across elevations, restoration and management of R. muscosa will require preserving LITERATURE CITED habitat across a wide range of elevations. BASTIEN, H., AND R. LECLAIR,JR. 1992. Aging wood ACKNOWLEDGMENTS frogs (Rana sylvatica) by skeletochronology. Journal of Herpetology 26:222–225. We thank G. Matson of Matson’s Laboratory in BRADFORD, D. F., F. TABATABAI, AND D. M. GRABER. Montana for the laboratory analysis of the frog 1993. Isolation of remaining populations of the toes. J. Andersen, R. Grasso, V. King, I. Lacan, B. native frog, Rana muscosa, by introduced fishes in Meneken, E. Patton, K. Pope, and L. Vance Sequoia and Kings Canyon National Parks, Cali- assisted in field sampling and data summaries, fornia. Conservation Biology 7:882–888. CASTANET, J., AND E. M. SMIRINA. 1990. Introduction to and H. Preisler helped with statistical analysis. In the skeletochronological method in amphibians U.S. Forest Service sites, collection of R. muscosa and reptiles. Annales de Sciences Naturales, toes was permitted by the California Department Zoologie 11:191–196. of Fish and Game (SC-1748), and the permit also COGALNICEANU, D., AND C. MIAUD. 2003. Population required an additional special memorandum of age structure and growth in four syntopic amphib- MATTHEWS AND MIAUD—RANA MUSCOSA AGE AND GROWTH 993

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