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Reproduction by female bullsnakes (Pituophis catenifer sayi) in the Nebraska Sandhills.

Studies of reproductive ecology of snakes aspire to move beyond empirical descriptions of reproductive parameters to understanding interspecific and intraspecific patterns of variation in those parameters, as well as mechanisms behind that variation. our research has benefitted from application of concepts originally applied to birds (Drent and Daan, 1980), which has focused attention on the reproductive importance of resources acquired in the current year (income breeding) versus those acquired in previous years (capital breeding; Stephens et al., 2009). Subsequent studies of plants and animals make it clear that those strategies represent poles of a continuum (Jonssen, 1997; Stephens et al., 2009). For example, although recent research has demonstrated that snakes primarily are capital breeders, reproductive output in some species apparently is limited to only one of the two categories of use of resources (Reading, 2004; Gregory, 2006), whereas others use a combination of the two strategies (e.g., Bonnet et al., 2001; Reading, 2004). Some reproductive parameters respond more to variation in capital resources, while others respond more to income resources (Warner et al., 2008). Furthermore, there is reason to expect geographic variation along this continuum in the general reproductive strategy (and individual reproductive parameters) for a given taxon (e.g., Santos et al., 2005). Hence, it was with the goal of quantifying and understanding the basis of annual variation in reproductive traits of bullsnakes (Pituophis catenifer sayi) that this study was undertaken.

The bullsnake is a diurnal predator on mammals and birds (including eggs of birds; Iverson and Akre, 2001) and is distributed from northern Mexico to southern Canada (Sweet and Parker, 1990). Locally, it is often one of the most conspicuous snakes (Imler, 1945; Fitch, 1993) and reaches densities in the Sandhills of western Nebraska [less than or equal to] 7 adults/ha (J. Fox, pers. comm.). Despite the extensive range and high local densities, published reports on reproduction ([greater than or equal to] 21 to date) have been mostly anecdotal. No study including both size of eggs and clutches, with a sample >5 bullsnakes, is available (Fitch, 1999). Similarly, although the genus Pituophis spans >29[degrees] of latitude and 29[degrees] of longitude, only five studies of reproduction with samples of >10 females are available (Parker and Brown, 1980; Zappalorti et al., 1983; Burger and Zappalorti, 1991; Diller and Wallace, 1996; Shewchuk, 1996). However, three of those refer to one western subspecies and two others refer to the same eastern population.

Limited samples have hampered studies of natural history of most snakes, often precluding an understanding of variation in life-history traits and their correlates (Fitch, 1975; Madsen and Shine, 2001). Coincident with studies of turtles in the Sandhills of Nebraska (Iverson, 1991; Iverson and Smith, 1993; Iverson et al., 1997), we had the opportunity to examine large samples of bullsnakes from a single area over many years. These samples were extensive enough to permit not only a thorough description of reproduction in this population, but also to examine interannual variation in reproductive traits and undertake preliminary analyses of correlates of that variation. In conjunction with a review of the literature, these results also permitted an analysis of geographic variation in reproductive traits across subspecies, species, and the genus.

MATERIALS AND METHODS--Bullsnakes were made available to us as part of a predator-removal program during 1987-1999 (Imler, 1945) on Crescent Lake National Wildlife Refuge, Garden County, Nebraska. Descriptions of our study area (Imler, 1945; Gunderson, 1973) as well as the general region (Weaver, 1965; Bleed and Flowerday, 1990) have been published previously. At and between three marshes on the refuge (Smith, Gimlet, and Hackberry lakes; maximum distance apart was 12 km), snakes were captured by hand, salvaged as road kills, and trapped along drift fences following methods of Fitch (1951). Effort was not uniform among years or months. A sample of 1,278 field-collected bullsnakes was available to us. Annual samples were: 1987 (5 May-17 June, 34 snakes), 1988 (12 April-10 July, 131), 1989 (5 May-28 June, 63), 1990 (20 April-1 October, 243), 1991 (26 April-9 July, 67), 1992 (27 April-4 July, 153), 1993 (26 April-5 July, 272), 1994 (18 April-29 June, 305), 1998 (13 May-26 June, 8), and 1999 (13 May-27 June, 5). Of this sample, 248 females were frozen upon capture for dissection and 39 females (captured 8 May-27 June) were held through oviposition, but all living snakes were relocated to agricultural areas off the refuge.

Although it might be argued that the bullsnake-removal program at the refuge could induce density-dependent effects on life-history traits, our data suggest that this removal had little effect on overall densities. At the most intensive site of removal, where every bullsnake observed along a 1,100-m drift fence was removed or relocated for 8 consecutive years (Gimlet Lake), number of snakes captured during the same period each year did not decrease (e.g., 59 in 1987, 48 in 1989, 112 in 1992, and 73 in 1993).

Frozen snakes were thawed, weighed to the nearest gram, snout-vent length was measured to the nearest 0.1 cm, they were dissected, enlarged follicles were counted and measured (length in mm), and corpora lutea (if present) were counted. Mass of body for females refers to pre-nesting or total mass. Spent-mass of body was measured directly or estimated as mass of body minus mass of clutch, because spent-mass of body plus mass of clutch equaled gravid-mass in captives for which data were available. Sex was determined by cloacal probing (Schaefer, 1934), dissection or, for small thawed snakes, by injecting water into the tail to evert hemipenes of males. Females were assumed to be mature if they bore enlarged (>15 mm) ovarian follicles when collected in May or June. Our dissections suggested that some females of reproductive size apparently skipped reproduction in a given year. In addition, some females of adult size captured in May, that were maintained at 25-28[degrees]C and offered food (rodents) almost daily, did not produce eggs, and on dissection in early July, showed no ovulatory-sized follicles. Therefore, we defined females >90-cm snout-vent length that bore no enlarged follicle, corpus luteum, or oviducal egg when they were collected in early May-early July as non-reproductive.

Females held for oviposition were maintained until oviposition, after which they were remeasured. Eggs were measured within 4 h of oviposition and placed in plastic boxes containing moist sandy gravel (1988, n = 5 clutches) or vermiculite (1992, n = 2; 1993, n = 6; 1994, n = 16; 1998, n = 5; 1999, n = 5). Eggs were incubated in a closed, insulated building at 25 [+ or -] 3[degrees]C until mid-July when they were moved to Richmond, Indiana, and placed in an environmental chamber at 28 [+ or -] 0.5[degrees]C until hatching. These conditions for incubation seem reasonable given that eggs in a nest located in 2005 by telemetry (Iverson et al., 2007) were 26-31-cm underground and mean temperature of soil on the same hillside at 20-cm depth averaged 27.8[degrees]C during 15 June-15 August (n = 5,579 readings). Hatchlings were measured to the nearest 0.1 cm and 0.1 g within 72 h of hatching.

Although supplemental feeding in captivity could affect size of egg, hatchling, and clutch (Bonnet et al., 2001; Lourdais et al., 2003), captive females captured earlier in spring (8 May-25 May, n = 25), and potentially fed more than their wild counterparts, did not differ from those captured in early summer (25 May-27 June, n = 15) in any life-history trait we measured. These data were combined for analysis.

We used partial correlation analysis to remove effects of size of body on reproductive variables. In addition, despite criticisms of the use of ratios (e.g., Packard and Boardman, 1988) and because of their direct practical use in the field (unlike residuals), they were included in analysis for comparison to results of the partial correlation and to previously published data; statistical conclusions for both approaches were identical. Samples were compared using t-tests (for two samples) or ANOVA with post-hoc comparisons of means calculated using Fisher's (protected) least-significant differences with a = 0.05. Means are followed by [+ or -] 1 SD. All calculations were performed on MacIntosh hardware with Statview or SuperAnova software (Abacus Concepts, Berkeley, California).

For geographic comparisons, some missing reproductive parameters were estimated using specific regression equations based on the population in Nebraska. For example, given the high correlation between parameters such as length, width, and mass of egg, size of egg can be estimated with reasonable reliability (r = 0.98). This permitted inclusion of studies where mass of egg or body were not reported directly, and allowed a preliminary glimpse at geographic variation in reproduction not otherwise possible. Regression analyses of reproductive data from the literature were conducted with all available data (including samples with n = 1; compilation available from the senior author), and repeated with only those samples with n > 3. For the repeated analysis, all published data for P. m. lodingi (4 studies; 5 snakes) and for P. melanoleucus mugitus (5 studies; 6 snakes), respectively, were averaged to produce a single sample for these taxa.

Although a recent molecular study (Burbrink and Lawson, 2007) determined that the genus Pantherophis (New World ratsnakes) was paraphyletic with Pituophis and recommended synonymy of Pantherophis under Pituophis, subsequent work in the same lab (Pyron and Burbrink, 2009) has confirmed monophyly of both genera (Rodriguez-Robles and de Jestis-Escobar, 2000). Comparisons in this paper were made within the restricted definition of the genus Pituophis following Reichling (1995) and Rodriguez-Robles and de Jesus-Escobar (2000). They recognized six species: P. deppei (Mexico), P. lineaticollis (Mesoamerica), P. melanoleucus (pinesnakes; eastern USA; three subspecies, melanoleucus, lodingi,andmugitus), P. ruthveni (eastern Texas and Louisiana), and P. catenifer (central and western North America; 9-11 subspecies, including the bullsnake P. c. sayi on the Great Plains, the gophersnakes P. c. deserticola and P. c. affinis in basin and range states, and the others along the West Coast).

Because of the uneven geographic, taxonomic, and phylogenetic sampling represented by data in published literature and because interspecific phylogenetic relationships are not yet well resolved (Rodriguez-Robles and de Jesus-Escobar, 2000; Pyron and Burbrink, 2009), we were not able to apply the comparative-phylogenetic method (e.g., Martins, 2000) to our analyses of reproductive output.

RESULTS--The smallest five females with follicles >30 mm in length or with oviducal eggs (i.e., reproductive adults) were 88, 89, 91, 91, and 92-cm snout-vent length, confirming that at least some females mature at just under 90-cm snout-vent length. However, because some sexually mature females skip reproduction in a given year, it was not possible to estimate maximum size of immature females. Based on preliminary data on growth from this population (Iverson et al., 2008), females reach 90-cm snout-vent length on average at the age of 26.4 months, suggesting that females require >2 full seasons to reach maturity, with breeding commencing in the third season (ca. 32 months post-hatching) for some females.

Adult females typically emerge from hibernation in late April-early May with ovarian follicles already enlarged to > 15 mm long (Fig. 1). Follicles continue to enlarge through May until they reach ovulatory size in early June. Courtship (trailing, nudging, neck biting, or a combination of these) was observed on 5 and 9 May 1994 and 21 and 26 May 2001, and copulation was seen on 8 May 1994. During the first 2 weeks of June, reproductive females rarely were encountered (Fig. 1), presumably reflecting inactivity associated with ovulation. By mid-June, most reproductive females had oviducal eggs, corpora lutea, or both. However, only 79% of adults reproduced each year, with 64% of small adults (90-99-cm snout-vent length), 78% of medium-sized adults (100-109-cm snout-vent length), and 86-100% of large snakes (> 110-cm snout-vent length) reproducing in a given year (Table 1). In addition, frequency of reproduction varied 69-95% annually (Table 1) and was correlated positively with warmth of previous summer (e.g., July-August degree days >15.6[degrees]C, r = 0.92, P = 0.01, n = 6), but not with temperature in spring (e.g., March-June degree days, r = 0.66, P = 0.15) or temperatures in autumn (e.g., September-October degree days, r = 0.03, P = 0.98) of the previous year, or with temperatures in spring of the current year (r = 0.21, P = 0.69).

[FIGURE 1 OMITTED]

Of 39 females captured in May or June and held until oviposition, 38 laid eggs 10 June-13 July (mean date 28 June [+ or -] 8 days). The remaining female held eggs until 29 July. Excluding that female, average date of oviposition varied significantly among years ([F.sub.5,31] = 9.43, P < 0.01) and was inversely correlated with average daily minimum temperatures in May (Fig. 2), but not with mean daily maximum temperatures in May (r = 0.14, P = 0.80), degree days in May (r = 0.15, P = 0.78), or degree days in April (r = 0.48, P = 0.34).

Females with oviducal eggs (confirmed by dissection) were captured on 6 and 20 June 1991 and 23 June 1992, and a female radiotelemetered in 2005 laid eggs overnight 24-25 June (Iverson et al., 2007). Many others captured in mid-June probably had oviducal eggs, but were held to oviposit in captivity. Most of these females were captured in June as they attempted to cross drift fences at edges of meadows as they were moving up into sandhills, presumably where they would nest. Dates of collection for these females (and days until they oviposited in captivity) were 8 June 1988 (15 days); 17 (19 days) and 22 (26 days) June 1992; 21 (12 days), 22 (13 days), 24 (11 days), and 27 (11 days) June 1993; 19 June 1998 (7 days); and 27 June 1999 (7 days). The first post-ovipositing females (with fresh corpora lutea) captured in 1988 were on 26 June (2 females); in 1989, on 22 and 27 June; in 1990, on 28 June (3); in 1991, on 27 and 30 (3) June; in 1992, on 24, 26, and 30 June; in 1993, on 26 June (2) and 3 July (2); and in 1994, on 17 (2), 18 (2), 19 (2), 21, 23, 25 (2), and 28 (2) June. These data suggest that nesting is mid-June-early July.

Data for incubation and hatching were recorded for 28 clutches. Excluding clutches from 1998, incubation was 51-70 days (mean 56.9 [+ or -] 3.8 days; n = 25). Given the similarity between temperatures for incubation of captives and temperatures of soil near the depth of our only recorded nest (Iverson et al., 2007), these incubation times probably are similar to those in the field. However, clutches in 1998 were in an incubator at 28-29[degrees]C from time of laying until mid-July before transfer to Indiana and they hatched more quickly (after 47-52 days; mean = 49.8, n = 3). Hatching of an entire clutch usually took 2-3 days (75%) following first pipping; the remainder took 4 (21%) or 5 days. Excluding clutches from 1998, dates of hatching were 12 August-10 September (mean date 25 August [+ or -] 7.5 days; n = 25). The warmer incubation of clutches in 1998 resulted in early dates of hatching 28 July-5 August (mean date 2 August; n = 3).

Eggs that are in contact as they are laid adhere to one another to form a contiguous clump (e.g., Guthrie, 1926). Eggs laid by 39 captive females averaged 49.2 [+ or -] 6.9 mm in length (range 33.2-75.2, n = 347), 27.8 [+ or -] 2.3 mm in width (range 17.6-34.7, n = 356), and 22.5 g (n = 356; individual eggs in clusters could not be weighed). Average mass of egg for 57 eggs (representing 21 clutches and 5 years) that were laid individually (without contact with other eggs) was 23.33 [+ or -] 5.6 g (range 9.5-36.5).

Although length of egg was correlated with width of egg (r = 0.143, P < 0.01, n = 341), length of egg was more variable and explained only 2% of variation of width of egg. Length and width of egg (in mm) were each correlated with mass of egg (r = 0.86, P < 0.01 and r = 0.59, P< 0.01, respectively; n = 55), and length and width of egg were related to mass of egg by the equation mass of egg = 0.435 length of egg + 0.992 width of egg - 23.75 (r = 0.98, P < 0.01, n = 55).

Elongation of egg (length divided by width of egg) averaged 1.78 [+ or -] 0.28 (range 1.25-3.19, n = 342) and was correlated positively with mass of egg (r = 0.49, P< 0.01, n = 55). Mean elongation of all eggs in 39 clutches averaged 1.81 [+ or -] 0.28 and was correlated positively with mean mass of eggs in clutch (r = 0.46, P < 0.01), negatively correlated with size of clutch (r = -0.82, P < 0.01) and mass of clutch (r = -0.49, P < 0.01), and not related to size of body (snout-vent length or mass of body; r < 0.20, P> 0.22). Thus, eggs were more elongate in lighter clutches and in those with fewer and larger eggs.

[FIGURE 2 OMITTED]

Mean mass of eggs in clutch was correlated positively with gravid-mass of body (r = 0.37, P = 0.02, n = 39; Fig. 3), but not snout-vent length (r = 0.27, P = 0.10, n = 39) or spent-mass of body (r = 0.24, P = 0.14, n = 39). Although there was a tendency for size of egg to increase with size of body, the relationship was not significant. There was no annual variation in mean mass of eggs in clutch ([F.sub.5,33] = 1.09, P = 0.38), mean snout-vent length ([F.sub.5,33] = 2.06, P = 0.10), or mean mass of body ([F.sub.5,33] = 1.95, P = 0.11).

Relative mass of eggs (mass of egg divided by gravid mass of body) averaged 0.039 [+ or -] 0.010 (range 0.021-0.065, n = 39) and was correlated negatively with snout-vent length (r = -0.60, P < 0.01, n = 39), mass of body (r = -0.65, P < 0.01, n = 39), and spent-mass of body (r = -0.62, P < 0.01, n = 39). Relative mass of eggs ([F.sub.5,33] = 0.43, P = 0.83) and residuals of mass of egg regressed against mass of body ([F.sub.5,33] = 0.56, P= 0.73) did not vary among years.

Mean size of hatchling averaged 32.7-cm snout-vent length and 19.30-g mass of body (Iverson et al., 2008). Because eggs in a clutch typically are laid in a clump, it was not possible to correlate size of individual egg with size of hatchling. However, mean length of egg (r = 0.87, P < 0.01, n = 20), mean width of egg (r = 0.65, P < 0.01, n = 20), and mass of egg (r = 0.92, P< 0.01, n = 20) were correlated with mean mass of hatchling per clutch. Mean mass of body of hatchling for 20 clutches was not correlated with snout-vent length or mass of body of the mother (r < 0.21, P > 0.37).

[FIGURE 3 OMITTED]

Size of clutch based on oviposited eggs averaged 9.8 [+ or -] 2.2 (range 4-14, n = 39) and averaged 9.5 [+ or -] 2.1 (range 414, n = 49) when counts of corpora lutea (including those that oviposited) were included. Size of clutch estimated from counts of enlarged follicles (i.e., counts of the largest set of uniformly sized follicles > 15 mm long) averaged 9.4 [+ or -] 2.5 (range = 3-17, n = 116) and was not significantly different from that based on corpora lutea (t = 0.29, P = 0.78). Size of clutch was correlated positively with both snout-vent length (Fig. 4) and mass of body, whether based on counts of oviposited eggs (snout-vent length, r = 0.43, P = 0.01, n = 39; mass of body, r = 0.45, P < 0.01, n = 39), corpora lutea (snoutvent length, r = 0.48, P < 0.01, n = 49; mass of body, r = 0.47, P < 0.01, n = 44), or follicles (snout-vent length, r = 0.65, P < 0.01, n = 115; mass of body, r = 0.75, P < 0.01, n = 106). Further, for 48 females that were captured 19 April-10 May (spring), partial correlation analysis to remove the effect of snout-vent length revealed that relative mass of body in spring was correlated positively with relative number of enlarged follicles present (r = 0.40, P = 0.01). Thus, relatively heavy females tended to leave hibernation with relatively larger potential clutches.

Mass of egg was inversely correlated with size of clutch (r = -0.34, P < 0.01, n = 39). In addition, partial correlation analysis of size of clutch versus mass of egg to remove the effect of mass of body also showed a strong inverse correlation (r = -0.60, P < 0.01), suggesting a trade-off between size of clutch and size of egg in this population.

Size of clutch did not vary among years ([F.sub.5,33] = 0.65, P = 0.67) for oviposited clutches. However, for the larger dataset (n = 150), including size of clutch based on eggs, corpora lutea, and enlarged follicles, size of clutch did vary significantly among years ([F.sub.6,144] = 2.88, P = 0.01). Neither snout-vent length ([F.sub.7,391] = 1.23, P = 0.25) nor mass of body ([F.sub.6,352] = 0.54, P = 0.78) varied significantly among years despite the bullsnake-removal program, but because these measures ofsize were correlated with size of clutch, they may cloud our understanding of annual variation in size of clutch. Therefore, we examined residuals of the regression between mass of body and size of clutch in this larger dataset and determined that they also varied significantly among years ([F.sub.7,J42] = 2.83, P = 0.01). Further, average residual value by year was significantly correlated with degree days in April-May (r = 0.83, P = 0.04, n = 6, for years with samples >6), but not with rainfall in May-June (r = 0.60, P = 0.21), total rainfall for previous year (r = 0.06, P = 0.92), mean temperature during April-September in previous year (r = 0.21, P = 0.68), degree days in July-August for previous year (r = 0.57, P = 0.24), or degree days for previous October (r = -0.38, P = 0.45). This suggests that increased temperatures in spring (rather than conditions during the previous year) resulted in ovulation of more follicles.

[FIGURE 4 OMITTED]

Relative size of clutch (size of clutch divided by gravid-mass of body) for oviposited clutches averaged 1.6 [+ or -] 0.3 eggs/100-g mass of body (range 0.7-2.2, n = 39), did not vary by year ([F.sub.5,33] = 1.05, P = 0.41), and was correlated negatively with snout-vent length (r = -0.35, P= 0.03, n = 39), mass of body (r = -0.45, P = 0.004, n = 39), and spent-mass of body (r = -0.60, P< 0.01, n = 39). Relative size of clutch for all counts of size of clutch (i.e., corpora lutea and enlarged follicles) averaged 1.9 [+ or -] 0.5/100-g mass of body (range 0.7-3.4, n = 150).

Mass of clutch for 39 females that oviposited in captivity averaged 232 [+ or -] 63 g (range 102-420 g) and was correlated positively with snout-vent length (r = 0.61, P < 0.01), gravid-mass of body (Fig. 5), and spent-mass of body (r = 0.37, P = 0.02). However, it did not vary significantly among years ([F.sub.5,33] = 2.38, P = 0.06).

[FIGURE 5 OMITTED]

Relative mass of clutch (mass of clutch divided by gravid-mass of body) averaged 0.37 [+ or -] 0.06 (range 0.18-0.48, n = 39) and was not correlated with snout-vent length (r = -0.10, P = 0.54) or mass of body (r = -0.13, P = 0.43). Neither did relative mass of clutch vary among years ([F.sub.5,33] = 1.47, P = 0.23), nor did residuals of mass of clutch regressed against gravid-mass of body ([F.sub.5,33] = 1.83, P = 0.13). Relative spent-mass of clutch (mass of clutch divided by [gravid-mass of body minus mass of clutch]) averaged 0.59 [+ or -] 0.14 (range 0.22-0.93, n = 39) and was not correlated with snout-vent length (r = -0.08, P = 0.64) or mass of body (r = -0.09, P = 0.57). Neither did relative spent-mass of clutch vary among years ([F.sub.5,33] = 1.75, P = 0.15), nor did residuals of mass of clutch regressed against spent-mass of body ([F.sub.5,33] = 2.21, P = 0.08).

DISCUSSION--Female P. c. sayi in Nebraska mature at larger sizes (88-cm snout-vent length) than female P. c. deserticola (ca. 78-cm snout-vent length in Utah, Parker and Brown, 1980; ca. 81-cm snout-vent length in Idaho, Diller and Wallace, 1996; 69.5-cm snout-vent length in British Columbia, Shewchuk, 1996; 75-cm snout-vent length in western Colorado, Hammerson, 1999) or female P. deppei in Mexico (65-cm snout-vent length; Ramirez-Bautista et al., 1995), but smaller than females of P. ruthveni in Louisiana (ca. 120-cm total length, 106-cm estimated snout-vent length, Himes et al., 2002). However, maturity in P. m. melanoleucus in New Jersey apparently is reached at sizes similar to those in Nebraska; the smallest mature female reported by Burger and Zappalorti (1991) was 91-cm snout-vent length. Size at maturity in southern populations of P. melanoleucus is unknown. In general, there is a pattern of decreasing average size of adults with increasing latitude and longitude among populations of Pituophis (Fitch, 1985; Iverson et al., 2008).

Bullsnakes in western Nebraska apparently begin breeding during their third activity season (32 months post-hatching), but no data on age at maturity are available for other populations of P. c. sayi. Similarly, females of P. c. deserticola (in northern Utah) also mature at 32 months of age, as P. ruthveni apparently does in Louisiana (Himes et al., 2002). Studies of variation in age and plasticity of age and size at maturity in this widespread genus are needed.

The ovarian cycle of bullsnakes in Nebraska is a postnuptial-vitellogenesis, seasonal pattern (Aldridge, 1979; Seigel and Ford, 1987), with minimum ovarian size following ovulation in late spring, follicular development during summer and autumn, and follicular maturation the following spring. The follicular cycle has not been examined in any other population of bullsnakes, but a female captured in northeastern Colorado on 12 June had oviducal eggs (Hammerson, 1999), similar to bullsnakes in Nebraska. However, a female captured in southwestern Kansas on 3 June had 11 oviducal eggs (Marr, 1944) and a female from Texas laid eggs in captivity on 10 June (Tennant, 1984). These limited data suggest that individuals in southern populations may ovulate earlier than those that are more northerly.

The only other Pituophis for which data on the ovarian cycle are available is P. c. deserticola. Two females captured in western Colorado on 26 May and 4 June, respectively, had 4-cm-long and 3.5-4-cm-long follicles (Hammerson, 1999), similar to the pattern we documented (Fig. 1). In addition, ovulation occurs 1-25 June in Utah (Parker and Brown, 1980) and 1-20 June in Idaho (Diller and Wallace, 1996), about the same as in our study.

Failure of some mature females in Nebraska to reproduce every year is not surprising considering data from other studies, including those based on captives (Fitch, 1970). For a review of information about other snakes, see Seigel and Ford (1987) and Aldridge and Duvall (2002). Parker and Brown (1980) reported that one of [greater than or equal to] 20 female P. c. deserticola captured in Utah on 19 June was not gravid. Similarly, of31 adult-sized females dissected by Diller and Wallace (1996), only one was non-reproductive and they concluded that reproduction was essentially annual in Idaho. In British Columbia, Shewchuk (1996) estimated that only 62.5% of P. c. deserticola that he examined were gravid. Burger and Zappalorti (1992) noted that at least some female P. m. melanoleucus can nest every year, but that some do not appear at the nesting sites in a given year. However, they did not estimate what percentage skipped reproduction each year.

Frequency of reproduction increased with size of body in Nebraska and this pattern also has been noted in other snakes (e.g., Blem, 1982; Shine, 1986; Seigel and Ford, 1987; Aldridge and Semlitsch, 1992; Brown and Weatherhead, 1997; Greene et al., 1999; Madsen and Shine, 2001; Reading, 2004), but not all (Whittier and Crews, 1990; Madsen and Shine, 1996; Shine et al., 1998). However, this pattern is probably a result of a general correlation between size of body and stores of energy in snakes (e.g., Reading, 2004; Gregory, 2006), because reproduction in most species depends on resources obtained in previous years (so-called capital breeders; Shine, 2003; Winne et al., 2006). Our preliminary data suggest that frequency of reproduction also is correlated with warmth of previous summer, just as Whittier and Crews (1990) detected for Thamnophis sirtalis (common gartersnake) in Canada. Presumably, climate more directly affects frequency of reproduction in these snakes through its effects on availability and digestibility of prey (Lourdais et al., 2002). For example, Diller and Wallace (2002) reported that frequency of reproduction in Crotalus viridis (prairie rattlesnake) in Idaho was related to density of prey (mainly voles) in the previous year (Andren and Nilson, 1983). Perhaps, populations of small mammals (particularly voles) in Nebraska are larger in warmer years (e.g., Reed and Slade, 2009) allowing increased predation by bullsnakes (Iverson and Akre, 2001). This might result in increased reserves of fat on average (Bonnet and Naulleau, 1994; Madsen and Shine, 2001; Bonnet et al., 2001; Lourdais et al., 2002) and greater frequency of reproduction in the following year. However, warmer temperatures also could increase rate of intake, digestion, and assimilation of food irrespective of density of prey. Conversely, increased temperatures also carry potential costs of a higher metabolism (Lourdais et al., 2002). Because bullsnakes reproduce well in captivity (e.g., Fitch, 1970) and are oviparous (most research on allocation of energy to reproduction has been done on viviparous species), laboratory studies of allocation of energy and reproductive output in this species could be rewarding.

Fitch (1970) reported that two pinesnakes that had been in captivity for a long time (presumably P. m. melanoleucus) produced two clutches in the same year, 49-53 days apart. To date, there is no evidence that any Pituophis is capable of double-clutching in a single year in the wild.

Courtship in bullsnakes in western Nebraska was observed only in May, and it has been noted on 9 May in southwestern Nebraska (Iverson, 1975), 26 May in Iowa (Loomis, 1948), and 27 May in northeastern Colorado (Bauerle, 1972; Hammerson, 1999). Courtship in other populations of P. catenifer in the field has been recorded 3-23 May in British Columbia (Shewchuk, 1996) and on 30 May in Utah (Woodbury, 1941). Captives have been seen mating on 27 May in Utah (Woodbury, 1931), 7 June in Arizona (Gloyd, 1947), and 21 and 29 April in central California (Fisher, 1925). Pituophis m. melanoleucus has been reported to mate in May in New Jersey (Kauffeld, 1957; Zappalorti et al., 1983) and a pair was observed copulating on 28 May in Tennessee (Gerald and Holmes, 2004). Mating in autumn has been observed only once in the genus; P. m. lodingi on 28 September in Mississippi (Lee, 2007).

Our data (and those of Imler, 1945) indicate that nesting in bullsnakes in western Nebraska occurs midJune-early July, but that females held in captivity often nest later (Table 2). Insufficient data were available to test the hypothesis that southern bullsnakes nest earlier in the year than those farther north. Nesting may occur later in P. c. deserticola in British Columbia (21 June to first week in July; Shewchuk, 1996), southwestern Idaho (27 June-19 July; Diller and Wallace, 1996), northern Utah (24 June-[greater than or equal to] 2 July; Parker and Brown, 1980), northern Arizona (July; Dodge, 1938), and in many captives (Table 2), than in P. c. sayi. Egg-laying has been studied in P. m. melanoleucus; 228 nests were deposited during 17 June-14 July over a 13-year period in New Jersey (Burger and Zappalorti, 1992). Not only is this nesting season nearly the same as that for bullsnakes in western Nebraska, but the annual timing of egg-laying in both populations is related inversely to temperatures in spring (Burger and Zappalorti, 1992). Gravid females also have been collected on 9 July in Virginia (Mitchell, 1994) and 29 May-2 July in North Carolina (Palmer and Braswell, 1995). These data and those from captive records (although suspect; Table 2) suggest little latitudinal variation in timing of nesting in P. melanoleucus, as well as the genus as whole, which is surprising given the relationship between temperatures in spring and time of nesting within northern populations of P. c. sayi and P. m. melanoleucus.

Eggs of Pituophis apparently adhere to one another when laid (Lockwood, 1875; Van Denburgh, 1898; Lee, 1967; Reichling, 1982), but the adaptive significance of this clumping of such large eggs is unclear. Average size of eggs in P. c. sayi is similar to that in other subspecies of P. catenifer (Table 3). Eggs of eastern P. m. melanoleucus are larger and similar in size to those of P. deppei in northern Mexico; however, the southern P. melanoleucus mugitus produces eggs about twice the size of those in northern populations or taxa. Most surprising is that the southern species P. ruthveni produces the largest eggs in the genus, over twice as large as those of P. c. sayi, to which it is most closely related (Rodriguez Robles and de Jesus-Escobar, 2000). This suggestion of a decrease in size of egg with increased latitude is corroborated by the inverse relationship between mass of egg and latitude for all samples of Pituophis with n [greater than or equal to] 3(r = -0.63, P = 0.05, n = 10). This pattern also is evident across all data in published literature for P. c. sayi (r = -0.74, P = 0.02, n = 9) and P. melanoleucus (r = -0.69, P = 0.03, n = 10). Samples of P. catenifer from the southern basin and range states or the Pacific Coast were inadequate to test for this pattern in the West.

In Nebraska, bullsnakes exhibit a significant correlation between size of egg and size of body. Similarly, Cliburn (1978) suggested that size of egg and mass of body might be correlated positively for a small sample of P. m. lodingi from Mississippi, and the same trend was evident based on six P. c. deserticola from British Columbia (Shewchuk, 1996). We suspect that the pattern of a weak but significant correlation between size of egg and size of body probably characterizes any population of Pituophis with an adequate sample. This pattern also may extend across populations and species, because estimated mass of egg from 19 samples across various taxa was correlated with estimated mass of body (r = 0.71, P < 0.01; n = 19).

Size of offspring (egg or hatchling) tends to be weakly correlated (Plummer, 1984; Ford and Seigel, 1989; King, 1993; Madsen and Shine, 1996) or not related (Greene et al., 1999; Diller and Wallace, 2002; this study) to size of body within other snakes; one species (white-lipped snake Drysdalia coronoides) even exhibits a negative correlation (Shine, 1981). Unfortunately, this relationship often is ignored in studies of reproductive strategies in snakes (e.g., Dunham et al., 1988).

We could identify no evidence of annual variation in size of egg (either actual or relative) in Nebraska, suggesting that size of egg might be dictated primarily by size of body and little affected by environmental fluctuation. Unfortunately, annual variation in size of egg has not been studied in any other population of Pituophis. Indeed, annual variation in size of offspring (egg or hatchling) has been studied poorly in snakes in general (Seigel and Ford, 1987), although it has been documented for two oviparous species (rough green snake Opheodrys aestivus, among females, Plummer, 1983; brown water python Liasis fuscus, both within and among females, Madsen and Shine, 1996) and two viviparous species (T sirtalis, Gregory and Larsen, 1993; asp Vipera aspis, Bonnet et al., 2001). Unfortunately, the basis for this variation in those species is unclear. For example, in the laboratory, Seigel and Ford (1991, 1992) demonstrated that variation in intake of energy had no effect on size of offspring in an oviparous (red cornsnake Pantherophis guttatus) and a viviparous snake (checkered garter-snake Thamnophis marcianus). Furthermore, we detected no difference in mass of egg (F1,37 = 0.33, P = 0.57) or body-size-standardized mass of egg (F137 = 0.11, P = 0.75) between female bullsnakes captured earlier in spring and fed ad libitum versus those captured later and fed less. However, intake of energy immediately prior to ovulation had a significant effect on size of offspring in a field study of a viviparous species (Bonnet et al., 2001). Clearly, more attention must be devoted to annual variation in size of offspring and its correlates in snakes before any universal pattern emerges, except that size of offspring tends to vary less than size of clutch.

Relative mass of eggs averaged 0.051 [+ or -] 0.018 (range 0.022-0.099) among 19 populations of Pituophis and is remarkably constant among taxa (Table 4). Relative mass of eggs for Pituophis is similar to that of other oviparous colubrids calculated from data compiled by Dunham et al. (1988; mean 0.047, n = 17 taxa). Unlike non-standardized mass of egg, neither relative mass of eggs (r = 0.32, P = 0.19, n = 19) nor residuals of mass of egg regressed on mass of body (r = 0.04, P = 0.87, n = 19) were related to latitude among populations of Pituophis. Unfortunately, no study of geographic variation in body-size-standardized mass of egg is available for other species of snakes.

Elongation of egg has not been examined previously in any Pituophis, but it is not related to size of body in Nebraska, although heavier clutches and those with fewer eggs tended to contain more elongate eggs. In addition, larger eggs tended to be more elongated. This suggests that females increase size of egg by adding to length (rather than to width), and that increases in size of clutch result in a relative shortening of individual eggs in the clutch. Unfortunately, we have neither data on possible differences in energy-content (nor eventual size of offspring) for elongated eggs versus those more shortened, nor has elongation of egg and its correlates been investigated in other snakes. Iverson et al. (2004) has discussed this subject relative to lizards.

Size of clutch in Pituophis is 2-24 eggs and exhibits considerable geographic and taxonomic variation (Table 5) with no obvious latitudinal or longitudinal pattern. Fewest eggs per clutch (4) are produced by P. ruthveni, despite its recent divergence from P. c. sayi, which has among the largest clutches in the genus (mean 12.9 for 21 samples; Table 5). Fitch (1970) speculated that there is a slight increase in size of clutch with latitude in Pituophis. There does appear to be a trend for an increase in size of clutch with latitude in P. melanoleucus (Table 5), but populations of P. catenifer in the basin and range states and along the West Coast seem to exhibit the reverse pattern, and no pattern is evident across the range of P. c. sayi. Regrettably, samples are inadequate to test these possible latitudinal patterns statistically. For 25 species of snakes, Fitch (1985) reported that 60% exhibited a latitudinal increase in size of clutch and 36% had a latitudinal decrease. Ofthe seven oviparous species in his sample, five exhibited a latitudinal increase in size of clutch, one a latitudinal decrease, and the seventh (a composite of P. melanoleucus and P. catenifer) exhibited no trend. Unfortunately, these patterns are clouded because of effects of size of body on size of clutch.

Fitch (1970, 1985) also suggested that size of clutch in Pituophis in the United States was highest in mid-continent, with reductions in populations near either coast (Table 5). For samples from the USA and Canada with n [greater than or equal to] 3, plains populations of P. c. sayi (mean 11.3, n = 5) had a significantly larger size of clutch ([F.sub.2,10] = 8.26, P = 0.01) than eastern P. melanoleucus (mean 7.9, n = 5), P. catenifer from basin and range states (mean 7.9, n = 6), or P. catenifer from the West Coast (mean 7.1, n = 2). Most snakes that have been studied tend to exhibit a decrease in size of clutch with longitude in the USA (Fitch, 1985), but this pattern also is complicated by a decrease in size of females with longitude in many of those species.

Size of clutch was correlated with snout-vent length within populations of P. melanoleucus in New Jersey and Mississippi (Burger and Zappalorti, 1991; Cliburn, 1978), as well as within populations of P. c. sayi (this study) and P. c. deserticola in Idaho (Diller and Wallace, 1996), Utah (Parker and Brown, 1982), and British Columbia (Shewchuk, 1996). However, no relationship between size of clutch and size of body (snout-vent length or mass of body) was evident across samples of Pituophis (e.g., snout-vent length, r = 0.08, P = 0.68, n = 28), nor just those with n > 3(r = -0.24, P = 0.45, n = 12), nor for any unrestricted or restricted sample within species or longitudinal region. A positive correlation between size of clutch and size of body is typical both within and among most populations of snakes (Fitch, 1970; Seigel and Ford, 1987; Dunham et al., 1988; Shine et al., 1998), but not all (Shine, 1981; and Aldridge and Semlitsch, 1992).

Size of clutch (and relative size of clutch) for bullsnakes in Nebraska varied annually, as frequently is true for snakes (Seigel and Fitch, 1985; Seigel and Ford, 1987; Aldridge and Semlitsch, 1992), although not always (Gregory and Larsen, 1993; Madsen and Shine, 1996; Greene et al., 1999). Seigel and Fitch (1985) detected larger clutches in wet years than in dry years in ring-necked snakes (Diadophis punctatus, oviparous), common gartersnakes (T. sirtalis, viviparous), and copperheads (Agkistrodon contortrix, viviparous), but not in plains gartersnakes (Thamnophis radix, viviparous). Seigel and Ford (1991, 1992) demonstrated that increased rates of pre-ovulation feeding resulted in larger clutches in both red cornsnakes (Pantherophis guttatus, oviparous) and checkered gartersnakes (Thamnophis marcianus, viviparous). Furthermore, Bonnet et al. (2001) and Lourdais et al. (2002, 2003) reported that size of clutch in the asp (V. aspis, viviparous) was influenced by both short-term (preovulatory) and long-term (prior year) storage of energy. Conversely, Santos et al. (2005) demonstrated no difference in body-size-standardized size of clutch among three populations of the oviparous viperine watersnake (Natrix maura) with significant differences in availability of food.

Size of clutch in bullsnakes seems to respond to intake of energy as in Vipera. Relatively heavier females in early spring already have greater numbers of enlarged follicles than more emaciated females, suggesting that size of clutch is influenced in part by energy accrued in previous years (i.e., capital breeders; e.g., Shine, 2003). In addition, size of clutch in bullsnakes varied with temperatures in spring (April-May), suggesting that short-term, warmer temperatures in spring may increase populations of prey, rates of intake of prey, or both, to increase storage of energy and final size of clutches. Of course, warm conditions also may only increase mobilization ofstored energyto small-yolked follicles and increase size of clutch by that means. Conversely, for our ovipositing females captured earlier in spring (prior to ovulation and fed ad libitum), there was no difference in size of clutch ([F.sub.1,37] = 0.84, P = 0.37) or body-size-standardized size of clutch ([F.sub.1,37] = 2.02, P = 0.16) compared to females captured late in spring (presumably near or after ovulation). It is possible that conditions for our captives were similar enough to those experienced in the field that no differential effect of excess food was produced in captivity. Alternatively, this pattern could have resulted from differences in stress in captivity. Clearly, future comparative studies of reproduction in other populations of Pituophis are needed. Experiments in both field and laboratory will be necessary to clarify the basis for annual variation in size of clutch that we observed in the field.

Relative size of clutch averaged 1.60/100-g mass of body in our population of P. c. sayi, 1.62 among six samples of P. c. sayi, 1.71 among 12 samples of P. catenifer, and 1.57 (range 0.34-10.29) among all 28 samples of Pituophis (Table 4). Despite consistency of these means, relative size of clutch does vary significantly among populations. Most unusual is the value of 10.29 for P. d. deppei in southern Mexico (Table 4), particularly given the value of 0.86 for the conspecific population of P. d. jani in northern Mexico. Similarly, relative size of clutch for P. ruthveni was estimated as 0.43 from the single clutch known for that taxon (Reichling, 1988), significantly lower than the mean for its closest relative P. c. sayi (1.62; two-tailed t = 3.94, P= 0.01).

Despite the dearth of data for relative size of clutch, clutches do tend to increase with latitude among P. melanoleucus (relative size of clutch, r = 0.68, P = 0.01, n = 13; residuals of size of clutch versus mass of body, r = 0.56, P = 0.05; n = 13), the only taxon with good latitudinal representation. This pattern was not evident for any other taxon or longitudinal sample (Table 4). Because this is the first examination of relative size of clutch in a snake, comparisons with other species are not possible; however, analyses of geographic variation in relative size of clutch are needed to test latitudinal, longitudinal, and altitudinal patterns in size of clutch in snakes presented by Fitch (1985).

Our data for Nebraska revealed an inverse correlation between size of egg and size of clutch. No previous study has examined this possible trade-off in another population of Pituophis. However, our partial correlation analysis of data for size of egg and size of clutch for six P. c. deserticola from British Columbia (Shewchuk, 1996) with the effect of mass of body removed revealed a non-significant trend toward such a trade-off (r = -0.75, P = 0.09). Unfortunately, the small sample in Shewchuk (1996) and the lack of data from any other population preclude identification of a consistent pattern within populations or taxa.

Many viviparous snakes exhibit an inverse correlation between size of offspring and size of clutch after the effect of size of body has been removed (Ford and Killebrew, 1983; Gregory and Larsen, 1993; King, 1993), but many others exhibit no such pattern (Plummer, 1992; Greene et al., 1999; Diller and Wallace, 2002). Perhaps, this tradeoff is more typical for oviparous species (Ford and Seigel, 1989; Madsen and Shine, 1996; this study), although this conclusion is hampered by failure of most studies to standardize for size of body when correlating size of egg and size of clutch.

Mass of clutch varies in Pituophis from 70 g in a P. c. deserticola from southwestern Idaho (Diller and Wallace, 1996) and 88 g in a P. d. jani from northern Mexico (Lazcano et al., 1993) to 689 g in a P. m. mugitus from Florida (Lee, 1967) and an estimated 730 g in a P. c. affinis from Arizona (Gloyd, 1947). For seven samples of P. melanoleucus, mass of clutch averaged 357 g, and for 11 samples of P. catenifer it averaged 299 g. In Nebraska, mass of clutch was correlated positively with size of body, as it was in P. c. deserticola in British Columbia (Shewchuk, 1996). This pattern is the logical expectation for any population of snakes (Seigel et al., 1986).

Relative mass of clutch averaged 0.37 (range 0.18-0.48) at our site, 0.39 across all samples of Pituophis (range 0.23-0.52, n = 19), 0.42 for all samples of P. catenifer, and 0.38 for all samples of P. melanoleucus (Table 4). It is clear that more variation in relative mass of clutch occurs within than among populations and that means for populations are remarkably constant across the range of the genus.

Relative mass of clutch in Pituophis is typical of that for other oviparous colubrids (0.34 for 43 samples in Seigel and Fitch, 1984; 0.32 for 18 samples in Dunham et al., 1988). Excluding the outlying P. d. jani (Table 4), neither relative mass of clutch (r = 0.40, P = 0.10, n = 18) nor residuals of mass of clutch regressed on mass of body (r = 0.05, P = 0.92, n = 18) were correlated with latitude. No other study has examined latitudinal variation in relative mass of clutch within or across species of snakes; we predict that such a correlation may be rare (Iverson et al., 1993). Relative mass of clutch did not vary with size of body in our population or within P. c. deserticola in British Columbia (Shewchuk, 1996). Similarly, Seigel et al. (1986) detected no such correlation within nine populations of snakes, including two other oviparous colubrids, or across 16 populations of oviparous snakes (Seigel and Ford, 1987). They argued that the lack of an effect of size of body on relative mass of clutch is expected given that the usual ecological correlates of relative mass of clutch (e.g., foraging strategy, reproductive mode, and escaping behavior) do not change during the lifetime of an adult.

Annual variation in relative mass of clutch has not been examined previously in Pituophis, but none was evident in our sample and we detected no difference in body-size-standardized mass of clutch (relative mass of clutch [F.sub.1,37] = 2.80, P = 0.10; residuals of mass of clutch and mass of body, [F.sub.1,37] = 1.90, P = 0.17) between females captured earlier in spring and fed ad libitum versus those captured later and fed less. Similarly, Seigel and Fitch (1984) reported no annual variation in relative mass of clutch for two viviparous and two oviparous species, and Madsen and Shine (1996) detected none within or among oviparous water pythons (Liasis fuscus). These data suggest that relative mass of clutch may be under strong selection as a species-specific, life-history trait (i.e., heavily genetically influenced). However, the only study to address plasticity in relative mass of clutch directly, revealed that providing a high-energy diet to captive red cornsnakes (Pantherophis guttatus, oviparous) resulted in increased relative mass of clutch (Seigel and Ford, 1991). Clearly, more research on proximate factors affecting relative mass of clutch (e.g., condition of body) is needed. In the future, we need to collect data on the full suite of life-history traits (including data for size of egg), as well as submit those data to more complete and appropriate analyses (including standardization of size of body), and we need to begin to examine the relationships of specific climatic and geographic variables to reproductive output in snakes rather than focusing simply on latitude and longitude (Hawkins and Dinz-Filho, 2004).

Managers F. Zeillemaker, K. Brennan, M. Heisinger, R. Huber, B. Behrends, L. Malone, S. Knode, and N. Powers at Crescent Lake Refuge permitted research and allowed access to samples of bullsnakes, and nearly the entire staff contributed to the project. Permits were provided by M. Fritz of Nebraska Game and Parks Commission. J. Fox and J. A. Rodriguez-Robles shared unpublished literature, J. Rodriguez, H. Smith, and K. Adler provided references, P. Baker assisted with climatic data, and E. Gonzalez Akre provided the resumen. Support was provided by Earlham College, Joseph Moore Museum of Natural History, Howard Hughes Medical Institute, Ford Foundation, Sears Roebuck Foundation, and the National Science Foundation. R. Seigel, R. Shine, and R. Smith provided valuable comments on early drafts. P. Dooley and D. Greene assisted in preparation of the manuscript.

Submitted 10 February 2010. Accepted 14 July 2011.

Associate Editor was Geoffrey C. Carpenter.

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John B. Iverson, * Cameron A. Young, Thomas S. B. Akre, and Christopher M. Griffiths

Department of Biology, Earlham College, Richmond, IN 47374 (JBI)

Center for Snake Conservation, 1581 Ridgeview Drive, Louisville, CO 80027 (CAY)

Department of Biological and Environmental Sciences, Longwood University, Farmville, VA 23909 (TSBA)

Walkersville Veterinary Clinic, 10559 Glade Road, Walkersville, MD 21793 (CMG)

* Correspondent: johni@earlham.edu
TABLE 1--Percentage of female bullsnakes (Pituophis catenifer sayi)
of various sizes in the Sandhills of Nebraska that were reproductive
in a given year.

                    1988               1989
Snout-vent
length (cm)   n     Percentage    n    Percentage    n

  90-99        2          100     1            0     7
  100-109     10           90     4          100     3
  110-119      9          100     3          100     1
  120-129      1          100     4          100     0
  130-139      0           --     0           --     1
Total         22           95    12           92    12

              1991               1992
Snout-vent
length (cm)   Percentage    n    Percentage    n

  90-99              86     9           89    12
  100-109            67    11           82    19
  110-119           100    10          100    20
  120-129            --     3          100    10
  130-139           100     0           --     3
Total                83    33           91    64

              1993               1994
Snout-vent
length (cm)   Percentage    n    Percentage

  90-99              67    24           46
  100-109            63    26           81
  110-119            70    15          100
  120-129            70     4          100
  130-139           100     1          100
Total                69    70           74

                     Total
Snout-vent
length (cm)    n     Percentage

  90-99        55           64
  100-109      73           78
  110-119      58           89
  120-129      22           86
  130-139       5          100
Total         213           79

TABLE 2--Records of date of oviposition for captive Pituophis. Sources
are listed by decreasing latitude within taxa.

                          Date captured or
 Taxon and location     number in captivity      Date of oviposition

Pituophis melanoleucus melanoleucus

  New Jersey            1 captive              9 July
  New Jersey            2 captives             12, 13 July
  New Jersey            9 June                 28 June
  New Jersey            2 captives             5 February, 28 April
  New Jersey            1 captive              15 May
  New Jersey            28 captives            4 November,
                                                 1 February-17 May
  Virginia              1 road-killed          9 July
  North Carolina        29 May-2 July          19 June-27 July

Pituophis melanoleucus lodingi

  Mississippi           26 June                14 July
  Mississippi           1 captive              29 May
  Mississippi           2 captives             3, 7 June

Pituophis melanoleucus mugitus

  Florida               16 June                27 June
  Florida               1 captive              7 July
  Florida               3 captives             21 June, 21 July,
                                               8-Aug

Pituophis catenifer sayi

  North Dakota          2 in June              16, 24 July
  Eastern Nebraska      25 June                26 July
  Nebraska              1 captive              15 July
  Kansas                3 captives             21, 22, 27 June
  Kansas                1 captive              27 June
  Kansas                2 captives             7, 11 July
  Kansas                1 captive              14 July
  Kansas                16 June                4 July
  Colorado              13 June, 8 July        16, 15 July
  Missouri              2 captives             15, 29 July
  Oklahoma              1 captive              1 July
  Texas                 1 captive              10 June
  Texas                 1 captive              28 July

Pituophis ruthveni

  Louisiana             2 captives             29 May, 11 June
  Louisiana             22 July                4 July

Pituophis deppei jani

  Northern Mexico       2 captives             14 May-7 June
                          (6 clutches)

Pituophis catenifer deserticola

  Utah                  ? captives             18 June
  Utah                  ? captives             10 July
  British Columbia      Late May               30 July, 4 August
  New Mexico            9 May                  1 July
  New Mexico            2 captives             2, 3 July

Pituophis catenifer affinis

  Arizona               Wild-bred              29 June
  Arizona               ? captives             7 July

Pituophis catenifer catenifer

  Central California    Captive                7 August

Pituophis catenifer annectens

  Southern California   10 wild-bred           7 July-16 August
  Southern California   5 captives             Early as 27 May
  Southern California   2 captives             16 April-10 July
                          (26 clutches)          (mean 28 May)

 Taxon and location               Source

Pituophis melanoleucus melanoleucus

  New Jersey            Conant and Bailey (1936)
  New Jersey            Conant and Downs (1940)
  New Jersey            New (1953)
  New Jersey            Wright and Wright (1957)
  New Jersey            Hine (1980)
  New Jersey            Fitch (1970)
  Virginia              Mitchell (1994)
  North Carolina        Palmer and Braswell (1995)

Pituophis melanoleucus lodingi

  Mississippi           Cliburn (1978)
  Mississippi           Reichling (1982)
  Mississippi           Hammock (1984)

Pituophis melanoleucus mugitus

  Florida               Iverson (1978)
  Florida               Iverson (1978)
  Florida               Neill (1951)

Pituophis catenifer sayi

  North Dakota          Wheeler and Wheeler (1966)
  Eastern Nebraska      Iverson (1975)
  Nebraska              Hudson (1942)
  Kansas                Fitch (1999)
  Kansas                Mehrtens (1952)
  Kansas                Gloyd (1928)
  Kansas                Collins (1982)
  Kansas                Gloyd (1928)
  Colorado              Hammerson (1999)
  Missouri              Anderson (1965)
  Oklahoma              Carpenter (1958)
  Texas                 Tennant (1984)
  Texas                 Treadwell (1962)

Pituophis ruthveni

  Louisiana             Reichling (1990)
  Louisiana             Lodrigue (2008)

Pituophis deppei jani

  Northern Mexico       Lazcano et al. (1993)

Pituophis catenifer deserticola

  Utah                  Hardy (1938)
  Utah                  Woodbury (1931)
  British Columbia      Shewchuk (1996)
  New Mexico            Degenhardt et al. (1996)
  New Mexico            Degenhardt et al. (1996)

Pituophis catenifer affinis

  Arizona               Klauber (1947)
  Arizona               Gloyd (1947)

Pituophis catenifer catenifer

  Central California    Fisher (1925)

Pituophis catenifer annectens

  Southern California   Klauber (1947)
  Southern California   Klauber (1947)
  Southern California   Fitch (1970)

TABLE 3--Average size of eggs of Pituophis based on the published
literature; number of sources included in calculating the average and
the range are in parentheses.

           Taxon                  Length (mm)         Width (mm)

P. melanoleucus melanoleucus    56.6 (8; 46-85)     34.5 (7; 22-45)
P. melanoleucus lodingi         76.9 (3; 62-88)     40.9 (2; 39-44)
P. melanoleucus mugitus         98.8 (2; 83-118)    38.6 (2; 28-52)
P. ruthveni                    119.0 (1; 100-130)   36.0 (1; 30-40)
P. catenifer sayi               52.3 (9; 42-72)     32.0 (9; 27-42)
P. catenifer deserticola        55.6 (2; 40-71)     27.9 (2; 17-30)
P. catenifer affinis            51.0 (1; --)        35.0 (1; --)
P. deppei jani                  62.5 (1; --)        30.3 (1; --)

           Taxon                   Mass (g)

P. melanoleucus melanoleucus   35.8 (7; 20-74)
P. melanoleucus lodingi        52.0 (2; --)
P. melanoleucus mugitus        87.4 (2; 42-133)
P. ruthveni                    63.7 (1; --)
P. catenifer sayi              29.8 (10; 10-40)
P. catenifer deserticola       24.4 (3; 11-34)
P. catenifer affinis           33.2 (1; --)
P. deppei jani                 33.5 (1; --)

Table 4--Average reproductive outputs of Pituophis) n (studies) =
number of sources; n (clutches) = number of clutches.

                                     n           n        Relative size
            Taxon                (studies)   (clutches)     of clutch

East Coast
  P. melanoleucus melanoleucus      4-6         4-6           1.14
  P. melanoleucus lodingi           2-4         2-5           0.73
  P. melanoleucus mugitus           2-3         2-3           0.66
Central
  P. catenifer sayi                 5-6        46-47          1.62
  P. ruthveni                        1           1            0.43
  P. deppei jani                     1           6            0.86
  P. deppei deppei                   1           4            10.29
Basin and range
  P. catenifer deserticola          3-4         42+           1.94
  P. catenifer affinis               1           1            1.47
  West Coast
  P. catenifer catenifer             1           1            1.58

                                 Relative mass   Relative mass
            Taxon                   of egg         of clutch

East Coast
  P. melanoleucus melanoleucus       0.045           0.41
  P. melanoleucus lodingi            0.050           0.37
  P. melanoleucus mugitus            0.062           0.33
Central
  P. catenifer sayi                  0.050           0.44
  P. ruthveni                        0.069           0.27
  P. deppei jani                     0.031           0.23
  P. deppei deppei                    --              --
Basin and range
  P. catenifer deserticola           0.061           0.37
  P. catenifer affinis               0.022           0.49
  West Coast
  P. catenifer catenifer              --              --

                                 Relative mass of clutch to
            Taxon                    spent-mass of body

East Coast
  P. melanoleucus melanoleucus              0.70
  P. melanoleucus lodingi                   0.59
  P. melanoleucus mugitus                   0.51
Central
  P. catenifer sayi                         0.80
  P. ruthveni                               0.38
  P. deppei jani                            0.33
  P. deppei deppei                           --
Basin and range
  P. catenifer deserticola                  0.06
  P. catenifer affinis                      0.96
  West Coast
  P. catenifer catenifer                     --

TABLE 5--Variation in size of clutch among taxa in the genus Pituophis
compiled from sources in the published literature; n (studies) =
number of sources; n (clutches) = number of clutches.

                                                             Mean
            Taxon                n (studies)   Range   (across studies)

East Coast
  P. melanoleucus melanoleucus       11        3-24          8.5
  P. melanoleucus lodingi             4         6-8          6.9
  P. melanoleucus mugitus             5         4-9          6.1
Central
  P. catenifer sayi                  21        4-21          12.9
  P. ruthveni                         1          4           4.0
  P. deppei jani                      1        7-12          10.2
  P. deppei deppei                    1        14-22         18.0
Basin and Range
  P. catenifer deserticola            5        2-15          7.6
  P. catenifer affinis                2        8-22          15.8
West Coast
  P. catenifer catenifer              3        3-10          7.2
  P. catenifer annectens              3        3-19          11.2

            Taxon                n (clutches)   Mean (clutches)

East Coast
  P. melanoleucus melanoleucus       156              9.2
  P. melanoleucus lodingi             5               6.8
  P. melanoleucus mugitus             6               6.2
Central
  P. catenifer sayi                   87             11.3
  P. ruthveni                         2               4.0
  P. deppei jani                      6              10.2
  P. deppei deppei                    4              18.0
Basin and Range
  P. catenifer deserticola            64              6.8
  P. catenifer affinis                4              12.8
West Coast
  P. catenifer catenifer              6               6.8
  P. catenifer annectens              17              8.3
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Author:Iverson, John B.; Young, Cameron A.; Akre, Thomas S.B.; Griffiths, Christopher M.
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1USA
Date:Mar 1, 2012
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