Comparing Life Histories of the Shortest-Lived Turtle Known (Chicken Turtles, Deirochelys reticularia) with Long-Lived Blanding's Turtles (Emydoidea blandingii)
Abstract
Evolutionary theories predict major differences in life-history trait values of long- and short-lived organisms. Such comparisons have not been possible for chelonians because no short-lived turtle was known until research revealed that chicken turtles (Deirochelys reticularia; DR) have a maximum longevity of 21 yrs. Life-history trait values of DR females are 1) age at maturity of females = 5–6 yrs; 2) clutches per season = 1.6; 3) annual fecundity = 6–8 female eggs per female; 4) average juvenile survivorship from age 1 to maturity = 0.60; and 5) low average annual adult survivorship = 0.66. We compared DR with the very long-lived Blanding's turtles (Emydoidea blandingii; EB) in Michigan. Over 14 yrs with no mortality (the minimum age at maturity of EB), the maximum potential fecundity produced by a single female embryo and her mature female offspring was 5 female eggs for EB and 1040 eggs for DR. Comparisons of life table output for approximately stable populations of DR and EB resulted in cohort generation times of 7 and 37 yrs, respectively. The life-history prediction that short-lived organisms should produce smaller offspring was not supported. Average wet mass of eggs is 10 g (8.4–11.3 g) for DR and 12 g (10–14 g) for EB; and average wet mass of hatchlings is 7.3 g (6–9 g) for DR and 9.3 g (6–13 g) for EB. Both differences are smaller than expected based on the difference in longevity. Short-lived female DR have an unusual tactic of investing in high fecundity and making substantial body size-specific investment in large eggs, which may reflect why juvenile survivorship had greater influence on population change rates than did adult survivorship. In contrast, adult survivorship had the greatest influence on population change rates of EB. Comparison of cohorts of 1000 female DR and EB hatchlings highlights the differences in life histories of short- and long-lived turtles: all DR would be dead by the time the last female EB had reached maturity at 21 yrs of age.
Evolutionary life-history theories predict substantial differences in coevolved life-history trait values of short-vs. long-lived organisms (Williams 1966; Stearns 1976; Roff 1992). Differences in predicted life histories of short- and long-lived vertebrates are supported by the positive relationship between attainment of maturity and longevity in vertebrates (Charlesworth 1980; Dunham et al. 1989; Charnov and Berrigan 1990; Prothero 1993).
Early studies of life histories accumulated robust data on relatively short-lived organisms, but lack of similar data on long-lived organisms prevented critical comparisons (Wilbur 1975; Miller 1976). As data on life histories of turtles accumulated, a general life-history paradigm of long-lived species emerged that is characterized by 1) high annual adult survivorship, 2) long reproductive lifetime and longevity, 3) delayed sexual maturity, 4) low annual fecundity, 5) within- and among-year iteroparity, 6) low survivorship of embryos in nests, 7) high average juvenile survivorships from age 1 to maturity (i.e., delaying maturity requires higher juvenile survivorship for any hatchlings to reach adulthood), 8) no detectable increase in mortality or reduction in reproductive output in the oldest individuals, 9) negligible influence of adult growth on reproductive output, and 10) a significant influence of juvenile growth on variation in age and size at maturity within populations of freshwater turtles and captive-raised sea turtles (Moll and Legler 1971; Gibbons 1982; Wilbur and Morin 1987; Brooks et al. 1988; Congdon and van Loben Sels 1993; Congdon et al. 1993, 2000, 2001, 2003, 2013, 2018; Iverson and Smith 1993; Bjorndal et al. 2013). As robust data on long-lived turtles accumulated, the problem for comparative analyses among turtle species was reversed because no short-lived species was known.
Documenting that chicken turtles (Deirochelys reticularia; DR) have the shortest lifespans of any turtle known provided the first and currently only opportunity to make life history comparisons between short- and long-lived turtles. We combined data from a three-decade study (Gibbons 1969; Gibbons and Greene 1978) with shorter-term studies on the Savannah River Site (SRS) near Aiken, South Carolina (Congdon et al. 1983; Buhlmann et al. 1995, 2009; Buhlmann 1998; Buhlmann and Gibbons 2001) to document the longevity and life-history trait values of DR. We compared the suite of life-history trait values of short-lived DR with a maximum longevity of 21 yrs to the well-studied and much longer-lived Blanding's turtle (Emydoidea blandingii, EB) with a maximum longevity of 84 yrs (J.D.C., unpubl. data, 2016) on the E.S. George Reserve in southeastern Michigan (Congdon et al. 1993, 2000). Comparisons of the 2 species were used to test the following predictions from evolutionary life-history theories: short-lived chicken turtles would 1) mature earlier and have 2) higher juvenile growth rates, 3) higher annual reproductive output, 4) smaller offspring, and 5) lower average juvenile survivorship from age 1 yr to maturity than would the longer-lived EB; we also predict that 6) survivorship of nests is not related to the longevity of female DR and EB because, for most species, variation in nesting behaviors of turtles do not have a major influence on high rates of nest destruction by predators (e.g., 70%–90%; Spencer and Thompson 2003, 2005).
METHODS
Chicken Turtles. — Compared to many other species of turtles, shells of DR are relatively thin and the plastron lacks a kinetic hinge that allows individuals to withdraw their head and forelimbs into to the limited protection of the shell (Jackson 1978, 1988; Mitchell and Buhlmann 1991). The primary habitats of DR are shallow, seasonally ephemeral, and highly productive wetlands that support relatively rapid growth of juveniles and young adult females (Buhlmann 1995; Congdon et al. 2013). Populations of DR seldom occupy wetlands where large predators such as alligators frequently occur. All body sizes of DR are at risk from some terrestrial and aquatic predators that include raccoons, foxes, coyotes, otters, mink, and herons (Jackson 1988; Ewert et al. 2006). Gravid females remain in aquatic habitats when wetlands retain water in the fall, and females either return to wetlands after they nest or stay in terrestrial refuges.
Male DR mature at 2–3 yrs of age at 75-mm plastron length and females mature at 5–6 yrs of age at approximately 150-mm plastron length (Buhlmann et al. 2009). Female DR produce an average of 8.0 eggs per clutch, females frequently produce two clutches annually, and clutch size and egg size increase with body size (Congdon et al. 1983; Congdon and Gibbons 1985; Buhlmann et al. 2009). Nesting begins in late August, is interrupted by low winter temperatures, and then resumes in February through mid-March of the following spring (Cagle and Tihen 1948; Gibbons 1969; Gibbons and Greene 1978; Jackson 1988; Buhlmann et al. 1995). Females retain eggs in second clutches over the winter until they resume nesting in the following spring (Buhlmann et al. 1995; Buhlmann 1998). As a result, embryos in first- and second-clutch eggs remain in diapause for 8 and 1 mo(s), respectively, until spring temperatures promote development and growth in late spring (Ewert 1985; Jackson 1988; Buhlmann et al. 1995; Buhlmann 1998). Hatchlings emerge from nests during August (Gibbons and Greene 1978), overwinter in terrestrial refugia, and move to wetlands in the following spring, 12–18 mo after nest construction (Buhlmann et al. 2009).
Mark–recapture, Survivorship, and Reproduction. — Life-history trait values of DR and EB were determined using similar protocols. Individuals were given a unique combination of marks, drilled or filed into their marginal scutes (Gibbons 1969). At each capture, we recorded sex (i.e., juvenile [unknown sex], male, female), injuries, abnormalities, and mid-line plastron length (PL) or carapace length (CL). Age zero for all species was assigned as the period from nest construction to hatchling emergence from nests (i.e., hatchlings and yearlings = age 1). At first capture of older juveniles, age was assigned based on annuli counts, and at subsequent recaptures calculated as the age at first capture plus the number of years between first and subsequent recaptures.
During the reproductive season, gravid females were radiographed (Gibbons and Greene 1979; Hinton et al. 1997) to document clutch size (CS) and egg widths (EW) and to determine relationships between reproductive traits and body size (DR, n = 259 [Buhlmann et al. 2009] and EB, n = 1031 [McGuire et al. 2015]). Recapture histories, age of individuals, and reproductive data were used to document clutch frequency and size and age at maturity of females. Annual fecundity was calculated as the number of female eggs (average clutch size × clutch frequency/2) based on the assumption of an equal hatchling sex ratio. For DR, calculation of fecundity was also based on all females producing at least 1 clutch each year and 60% of females producing a second clutch, and for EB was based on 80% of females producing a single clutch in a given year.
Survivorship of embryos was measured from 21 DR nests produced from 1994 to 1996 at Dry Bay on the SRS (Buhlmann et al. 2009) and from 316 observed EB nests (1976–1998) on the University of Michigan Edwin S. George Reserve (ESGR) (Congdon et al. 2000; J.D.C., unpubl. data, 2007).
Juvenile and adult DR at Ellenton Bay (n = 690) and Dry Bay (n = 461) were assumed to have died during the year following their last capture. Annual survivorships of juveniles were calculated over 4 and 5 yrs at Dry Bay and over 12 yrs at Ellenton Bay. Juvenile survivorships from age 1–5 yrs were based on 690 individuals first marked as hatchlings. Adult survivorships were determined from 65 samples of known-age individuals and adults of unknown ages during a 31-yr period (1967–1997) at Ellenton Bay. Annual survivorships for all samples of individuals age x to age x + 1 were then averaged for each age. For comparisons between species, we calculated survivorships of adult male and female DR (at SRS) and EB (at ESGR) based on the intervals between first and last captures (Proc Lifetest, SAS Institute Inc 1998).
Life Tables and Life-History Comparisons Between Species. — Populations of DR on the SRS and of EB on the ESGR are well studied; however, where actual data on a specific life-history trait value was weak or absent for one or both species, we set boundaries on the values used in construction of life tables that supported reasonable comparisons between species (Dunham et al. 1989; Congdon et al. 1993, 1994). For example, juvenile survivorships of DR were well documented over all 5 yrs prior to maturation (Table 1), whereas age-specific juvenile survivorships of EB over their extended juvenile period (mean = 17 yrs; min–max = 14–21) remain unknown. Therefore, comparisons between species used average juvenile survivorships from age 1 to maturity for life table calculations.
Life table inputs are mx = annual fecundity (the number of female eggs per female), Sx or lx = age specific annual survivorships. Life table outputs include Sx or lx = the probability of survival from age x to age x + 1, lxmx = (lx × mx), r = the intrinsic rate of population increase, Tc = cohort generation time, and doubling or halving times = the number of years in which a population will increase (+) or decrease (–) by 50%.
We started with life tables representing relatively stable populations and compared how varying one life table input value at a time (while holding all others constant) influenced population change rates (i.e., the slopes of relationships between intrinsic rate of population change r). We also created a life table for DR based on data from both Ellenton and Dry bays. In addition, we explored how DR may compensate for the constraint of remarkably short reproductive and total lifespans compared with EB by calculating maximum potential fecundities for each species (with zero mortality of all age classes) over 14 yrs (the minimum age at maturity of EB).
RESULTS
Juvenile and Adult Growth Rates and Age and Size at Maturity. — Body sizes of adult female DR and EB were similar (Table 2a). Growth rate of juvenile DR (average from hatchling to maturity) is 3 times higher than that of the substantially longer-lived EB (Table 2). Average growth rates of juveniles were 11 and 12 times growth rates of adults for DR and EB, respectively (Table 2a). Female DR mature at 5–6 yrs of age and have maximum reproductive life spans of 15 yrs, whereas female EB mature at 17.5 yrs (min–max = 14–21 yrs) and have maximum reproductive life spans of > 60 yrs (Table 2a).
Embryo, Juvenile, and Adult Survivorship and Longevity. — Survivorships of embryos in nests were 0.27 for DR and 0.30 for EB (Table 2) and, based on data from Ellenton Bay, juvenile survivorship from age 1 (yearlings) to age 5 averaged 0.51 (Table 1). Average juvenile Sx from age 1 to minimum age at maturity (age 14) required to maintain a stable population for EB was 0.78 (Table 2b).
Annual adult Sx was 0.63 and 0.66 for female and male DR on the SRS, respectively (Tables 1 and 2b; Fig. 1) and was > 0.96 for female and male EB (Table 2b; Fig. 1). Annual adult Sx required for maintaining stable populations was 0.71 for DR and 0.96 for EB (Table 2b).
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 21, 1; 10.2744/CCB-1521.1
Over 32 yrs of study, the longest lifespan documented for 183 adult DR was 21 yrs (a 16-yr recapture interval as an adult plus a 5-yr juvenile period; Fig. 2). Only 26% of DR first captured as adults were recaptured 3 or more years later (Table 1; Fig. 2). After 13 yrs post–first capture as an adult, essentially all male and female DR were not recaptured and were assumed to be dead (Fig. 1); in contrast, > 50% of adult EB (Fig. 1) had survived. The longest-lived EB captured on the ESGR was a minimum of 84 yrs of age (J.D.C., unpubl. data, 2016).
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 21, 1; 10.2744/CCB-1521.1
Reproductive Traits. — Average clutch size, egg size, hatchling size, and hatchling wet mass of DR and EB were similar (Table 2a). Increases in clutch size with body size were similar for female DR (slope coefficient [CS] = 0.11, r2 = 0.15) and EB (CS = 0.10, r2 = 0.25), whereas the increase in egg widths (EW) was greater in DR (slope = 0.09, r2 = 0.46) than in EB (EW slope = 0.019, r2 = 0.03). Annual number of clutches was < 1.0 for EB (i.e., females produced a maximum of 1 clutch/yr and did not reproduce in all years). In contrast, DR females produced a first clutch in all years and 60% of females produced 2 clutches annually (i.e., clutch frequency = 1.6; Table 2a).
Following the type of life-history comparisons introduced by Cole (1954), we explored how the consequences of maturing at ages of 5 yrs (DR) vs. 14 yrs (EB) are illustrated by differences in reproductive potentials of a single female hatchling of both species (with no mortality) over their first 14 yrs of life. A single DR hatchling reaching maturity at age 5 yrs and producing her first 8 offspring, together with the reproductive output of her subsequent 120 daughters and granddaughters after they mature, would total 1040 female offspring (Table 3). An initial female hatchling EB would have matured and produced 5 female offspring. Thus, a single female DR's potential reproductive output over 14 yrs is 208 times that of a female EB. However, the difference in reproductive potential is substantially narrowed by differences in maximum reproductive lifetimes of 15 and 66 yrs for DR for EB, respectively.
Inputs and Output for Chicken Turtle Life Tables. — Overall clutch size of DR averaged 8.3 eggs (min–max = 2–16, n = 208) from 1969 to 1997 (Table 1) and annual reproductive frequency was 1.6 clutches per female. Clutch sizes averaging 7.3 eggs (min–max = 2–14, n = 96, 1977–1981) at Ellenton Bay and 9.9 eggs (min–max = 2–16, n = 88, 1994–1998) at Dry Bay were used to estimate low and high fecundities of 5.8 and 7.9 female eggs per female, respectively (Table 2a). Fecundity value used for a stable population life table was 8.4 female eggs per female (Table 2b). Input values based on data from DR populations on the SRS (Table 2b) resulted in a life table for a rapidly declining population (r = –0.17512, Tc = 6.7 yrs with a halving time of 4 yrs; Table 4a).
To allow comparisons among species, conservative adjustments to input values were made to result in life tables representing relatively stable populations of DR and EB (Table 2b). The cohort generation (Tc) for DR was 7 yrs (Table 4b) and for EB was 37 yrs (Congdon et al. 1993). The order of strength of influence of life-history trait values on population change rates (i.e., slopes of regression lines), from high to low, were juvenile Sx, adult Sx, and fecundity for DR and adult Sx, juvenile Sx, and fecundity for EB (Fig. 3a–f).
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 21, 1; 10.2744/CCB-1521.1
DISCUSSION
Lifespan of Chicken Turtles. — Four lines of evidence support the very short lifespan of adult DR: 1) only 2 individuals first captured on the SRS as hatchlings had recapture intervals longer than 10 yrs (i.e., ∼ 5 yrs as an adult); 2) fewer than 20% of young adults were recaptured after 4 yrs (Fig. 2); 3) the maximum first to last intercapture interval of adults was 16 yrs; and 4) the record longevity for DR in captivity at the Chicago Zoological Park was 14 yrs 8 mo (Slavens and Slavens 1997).
To set the stage for the magnitude of differences in life histories of short-lived DR and long-lived EB, comparison of survivorship of cohorts of 1000 hatchlings resulted in all DR dying before the last female EB reached maturity at 21 yrs of age (Fig.1). All but one of six predictions were supported.
1) Shorter-lived Turtles Mature Earlier (Supported).—Shorter-lived DR mature at approximately 5–6 yrs of age, and this results in hatching-to-maturity generation times up to 15 yrs shorter than for longer-lived EB (mean = 17.7, min–max = 14–21 yrs; Congdon and van Loben Sels 1993; Congdon et al. 1993, 2001). Costs of delaying maturity have to be offset by benefits derived from higher reproductive output, increased parental investment, or extended reproductive lifetimes (Williams 1966). High adult mortality rates of female DR place a high cost on delaying maturity by 1 yr. A female DR delaying maturity by 1 yr is exposed to a serious evolutionary cost of error (i.e., zero lifetime reproductive success) compared with female EB with a high probability of annual survival.
2) Short-lived Turtles Have Higher Juvenile Growth Rates (Supported). — Juveniles are smaller than adults and should make large investments in growth because body size is almost always associated with increased survivorship (Williams 1966). Growth rates of juvenile and adult females are higher for DR than for EB. Average growth rates of juvenile DR and EB from age 1–5 yrs were 29.5 and 13.4 mm/yr, respectively. A 16-mm/yr faster growth rate over 5 yrs would result in DR females being 64 mm larger than a 5-yr-old juvenile EB. Average growth rate of juvenile DR from age 1 to maturity (29.5 mm/yr) is approximately 3 times the growth rate of juvenile EB (9.3 mm/yr) from age 1 to minimum age at maturity of 14 yrs (Table 2a).
3) Short-lived Turtles Have Higher Annual Reproductive Output (Supported). — Early maturity and high investment in annual reproduction appear to be adaptive responses to a low probability of future reproduction imposed by high, extrinsic adult mortality (Williams 1966; Zera and Harshman 2001). As noted by Gibbons (1982), the most important mechanism for increasing fecundity for most species of turtles is higher clutch frequency. Although female EB have a slightly larger clutch size, DR have a higher annual reproductive output that may be supported in part by postponing nesting until August after the period of high wetland productivity. On the SRS, delaying the initiation of nesting results in a seasonal interruption of nesting activity in fall that places a substantial, if not absolute, temporal restriction on the ability of females to produce a third clutch of eggs. Reliance on high fecundity to maintain populations is supported by suggestions of production of a third clutch by some female DR in other areas of their range (Ewert et al 2006; McKnight et al. 2015, 2018). In contrast, EB females produce fewer than 1 clutch/yr but reproduce over many more years than do DR (Congdon et al. 2000).
4) Short-lived Turtles Have Smaller Offspring (Not Supported). — Although hatchling DR are slightly smaller than hatchling EB, the difference is smaller than expected based on the difference in longevity. Hatchling DR on the SRS average 31.9 mm CL (min–max = 28–35 mm), while hatchling EB on the ESGR average 35.2 mm CL (min–max = 30.0–38.8 mm; Table 2a). Average wet mass of eggs is 10 g (8.4–11.3 g) for DR and 12 g (10–14 g) for EB, and average wet mass of hatchlings is 7.3 g (6–9 g) for DR and 9.3 g (6–13 g) for EB (Table 2a). At six locations from South Carolina, south to Florida and west to Texas, female DR produce eggs that are similar in size, and this should result in similar-sized hatchlings (McKnight et al. 2018).
Hatchling DR on the SRS have substantially higher parental investment (i.e., percent lipids/body dry weight = 27.4%, n = 15 hatchlings; Congdon et al. 1983) than do hatchling EB (16%, n = mean of 2 clutches; Rowe et al. 1995). Egg and offspring size increases with female body size of shorter-lived DR (Buhlmann et al. 2009) and the much longer-lived EB, but the increase in egg size is less pronounced in longer-lived EB females (McGuire et al. 2015). However, indeterminate growth rates of young adult female DR are more rapid than in EB (Congdon et al. 2013), but growth of adults occurs primarily during the first 3 and 6 yrs following maturity for DR and EB, respectively (Congdon and van Loben Sels 1991; Buhlmann et al. 2009). Increased parental investment (large hatchlings with substantial lipid reserves) is a mechanism for fueling hatchling growth and increasing early juvenile survivorship, particularly during drought conditions (Buhlmann et al. 2009). Yearlings and young juveniles of both species are too small to escape most of the known predators (e.g., raccoons, foxes, weasels, mink, herons, crows, and probably shrews).
5) Early Maturing DR Have Lower Average Juvenile Sx (Supported). — Increasing age at maturity requires that Sx of hatchlings must increase enough to allow any hatchlings to reach maturity (Dunham et al. 1989; Congdon et al. 1993, 1994). The average juvenile Sx from yearling to maturity necessary to maintain a stable population was 0.60 for the early maturing DR and 0.78 for the late-maturing EB.
6) Survivorship of Nests Is Not Related to the Longevity of Female DR and EB (Supported). — In spite of the differences in nesting ecology and suites of predators, nest survivorships of DR (0.27) and EB (0.30) were similar (Table 2b). Rates of annual nest destruction by predators from 90% to 100% have been reported (Congdon et al. 1987; Spencer and Thompson 2003, 2005) and secondarily by hazards such as nest parasites, flooding, erosion, shading, and temperature extremes. In general, it is unlikely that female freshwater turtles in many locations can modify nest site selection based on predicting densities of predators or females of the same or other species nesting at a particular site or day of year. The unusual nesting season of DR (when no other syntopic turtles nest) may result in higher or lower nest depredation rates depending on a host of other variables (e.g., location, surrounding habitats, distances among wetlands, and rainfall determining quality of wetlands).
CONCLUSIONS
Chicken turtles occupy temporary wetlands, which results in a suite of high and variable risks. The thin shell of adult DR limits the type and number of seasonally fluctuating wetland habitats suitable for maintaining populations. Prolonged droughts result in increased mortality from desiccation, starvation, and increased encounters with terrestrial predators (Buhlmann and Gibbons 2001; Buhlmann et al. 2009), and emigration to permanent wetlands occupied by alligators may be a behavior of last resort.
Periods of high rainfall can result in temporary occupation of ephemeral wetlands by large alligators, increased visits from otters, and perhaps more-frequent visits by herons. The combination of risks faced by all ages of DR contributes to their reliance on early maturity, high fecundity, and unusual investment in large offspring as important mechanisms for population persistence.
A complex suite of reproductive tactics of females and the ability of hatchlings, juveniles, and adults to overwinter and aestivate on land are important in allowing DR to successfully occupy seasonal wetlands with unpredictable hydroperiods (Bennett et al. 1970; Buhlmann and Gibbons 2001; McKnight and Ligon 2020). Short adult lifespans of DR require high fecundity to attain adequate recruitment of juveniles at levels sufficient to maintain or recover populations. Conservation efforts should focus on increasing adult and juvenile survivorship of DR (predator control) and protection of surrounding core uplands used by females for nesting and aestivation by hatchlings, juveniles, and both sexes of adults (Buhlmann 1995; Semlitsch 1998, 2006; Buhlmann and Gibbons 2001; Semlitsch and Bodie 2003). Where possible, water levels in selected temporary wetlands should be maintained during severe droughts or during some years of extended droughts.
Producing proportionally more offspring late in life is the mechanism for evolution of traits that either delay the onset or decrease the severity of senescence (Williams 1957, 1966). Adult female EB can reproduce for more than 60 yrs, and the oldest females did not exhibit increased mortality or decreased reproductive output (i.e., actuarial senescence; Congdon et al. 2001; Miller 2001). In contrast, approximately 80% of female DR die by their fourth year as an adult (Fig. 1a), a mortality rate that severely restricts their ability to increase the proportion of late- to early life births (i.e., the evolutionary mechanism for delaying the onset of senescence). Large differences in longevities of DR and EB provide an excellent opportunity for a comparative study of aging and senescence in turtles.
Survivorship curves of chicken turtles (Deirochelys reticularia) and Blanding's turtles (Emydoidea blandingii) to age 14 yrs. Circles = females; triangles = males.
Maximum intercapture intervals of 183 adult chicken turtles (Deirochelys reticularia) over 33 yrs on the Savannah River Site.
Relative influence on rates of change from a stable population of (a–c) chicken turtles (Deirochelys reticularia), and (d–f) Blanding's turtles (Emydoidea blandingii). The largest influences are represented by the steepest slopes.
Contributor Notes
Handling Editor: Peter V. Lindeman
