2007 NORTHEASTERN NATURALIST 14(4):619–628 Hydroperiod and Metamorphosis in Small-mouthed Salamanders (Ambystoma texanum) Travis J. Ryan* Abstract - Ambystoma texanum (Small-mouthed Salamander) breeds primarily in temporary wetlands, and while natural history studies have suggested a minimum larval period of about 2 mo, it is not clear how hydroperiod (the length of time that a temporary wetland holds water) infl uences populations. I conducted a mesocosm experiment to investigate the effects of hydroperiod on the completion of metamorphosis, as well as age and size at metamorphosis. I used hydroperiods of 50, 75, and 100 d, and a non-drying treatment as a control. Survival to the end of each hydroperiod was consistent among all groups, but no individuals completed metamorphosis in the 50-d treatment. The proportion of individuals completing metamorphosis increased with longer hydroperiods, as did the age at metamorphosis. The size at metamorphosis, however, was not affected by the length of the hydroperiod. My results show that a minimum hydroperiod of 2.5 mo is necessary for populations of Small-mouthed Salamander. Maintenance of natural hydroperiods in wetlands under the threat of development is a critical consideration for the long-term persistence of Small-mouthed Salamander populations. Introduction Most experimental investigations of the timing of metamorphosis in amphibians focus on the size and age at metamorphic climax because of the importance of these variables in theoretical optimality models (e.g., Day and Rowe 2002, Werner 1986, Wilbur and Collins 1973) as they relate to reproductive success. While the age and size at metamorphosis can infl uence the age and size at fi rst reproduction (and thus adult fi tness; Semlitsch et al. 1988, Smith 1987), the timing of metamorphosis may at times be independent of future reproductive success. Selection has apparently favored phenotypic plasticity with regards to metamorphosis in species with unpredictable larval environments (Altwegg et al. 2002, Laurila et al. 2002, Leips et al. 2000). Hydroperiod, the length of time an ephemeral wetland retains water, may be one of the most important environmental factors for amphibians that use ephemeral wetlands as nuptial-natal sites (Semlitsch et al. 1996). Larvae must complete development and metamorphosis prior to the drying of the wetland or suffer desiccation and death (Rowe and Dunson 1993). Accelerated metamorphosis and catastrophic mortality from “early” drying are documented for many pond-breeding amphibians (Calef 1973, Tevis 1966), especially those breeding in desert environments (Newman 1988, 1989), but also those in intermittent or hydrologically unstable streams as well (e.g., some salamanders, such as Eurycea; Ryan and Bruce 2000). Even if the hydroperiod permits the completion of metamorphosis, it may *Department of Biological Sciences, Butler University, Indianapolis, IN 46208; tryan@butler.edu. 620 Northeastern Naturalist Vol. 14, No. 4 still infl uence the age and size at metamorphosis (Parris 2000), which may in turn infl uence adult fi tness (Semlitsch et al. 1988). While hydroperiod clearly has signifi cant effects at the individual and population level, it also infl uences community-level interactions (Semlitsch et al.1996, Snodgrass et al. 2000). The timing of inundation (pond-fi lling) can shape interspecifi c competition (Boone et al. 2002), and the length of the hydroperiod can infl uence predator-prey relationships as well (Rowe and Dunson 1995, Wellborn et al. 1996). Although the effects of hydroperiod are widely appreciated in a general sense (Phillips et al. 2002), details of how hydroperiod shapes the dynamics of metamorphosis is poorly understood for most individual species, even though such information is increasingly relevant for species-specifi c conservation. Ambystoma texanum Matthes (Small-mouthed Salamander) is common throughout the midwestern and south-central United States, where it breeds primarily in ephemeral wetlands (Petranka 1998). Like other ambystomatids, the Small-mouthed Salamander is at risk due to wetland destruction or conversion throughout its range. There are relatively few published accounts on the aquatic ecology of the Small-mouthed Salamander, leading to a rather vague understanding of its larval life history. Time to metamorphosis is generally considered to be 2–4 mo (Minton 2001, Petranka 1998) and appears to vary to some degree in response to hydroperiod (Phillips et al. 2002). The exact nature of the relationship is unknown, however. I conducted a mesocosm experiment to better defi ne how hydroperiod infl uences larval survival, completion of metamorphosis, and the timing of and size at metamorphosis in Small-mouthed Salamanders. Materials and Methods I used 1000-L cattle tanks as mesocosms for Small-mouthed Salamander populations. Each cattle tank was outfi tted with an external standpipe that limited the maximum depth in the tank to 35 cm. I fi lled the tanks with tap water on 12 March 2002, and on 14 March, I added approximately 1 kg of leaf litter and the fi rst of several aliquots of concentrated zooplankton mixture to each tank. Zooplankton communities were derived from Amos Ditch (see below) and a neighboring permanent pond, and zooplankton was added 2–3 times/week until 12 April. Zooplankton aliquots were examined to ensure they did not contain potential predators. Each tank also received one egg mass of a pond snail, Lymnea stagnalis L. (Great Pond Snail), collected from the vicinity of Amos Ditch. I left the cattle tanks uncovered to permit oviposition by insects. No predators (e.g., Anax or other dragonfl ies) became established in the tanks during the course of the experiment. I studied a natural population of Small-mouthed Salamanders that breeds in Amos Ditch, an ephemeral pond located within Eagle Creek Park, a ca 5200-ac municipal park of Indianapolis, IN. Oviposition and hatching are asynchronous in the Amos Ditch population. I observed freshly laid eggs from early February through early April. The fi rst hatchlings were evident prior to the appearance of the last-laid embryos. In early March, I obtained eggs from 2007 T.J. Ryan 621 5 mated females (caught in unbaited minnow traps) that were placed in 40-L plastic tubs in the lab; an additional female was placed outdoors in a cattle tank fi lled to a depth of approximately 10 cm. I removed eggs within 12 hr of oviposition and maintained them in the lab at approximately 18 °C with light aeration until hatching. In order to approximate natural hatching dynamics, I added a total of 40 hatchlings to the mesocosms as they hatched between 28 March and 12 April, introducing the same number of hatchlings to each tank at each addition. Hatchlings were haphazardly assigned to cups that were then randomly assigned to mesocosms. After day 40, I checked each tank daily between 2030–2330 hr for the presence of metamorphic individuals (metamorphs). Metamorphs were collected by hand with a small aquarium net. For comparative purposes, metamorphs with gills less than 1 mm were captured and kept in a small polyethylene dish in the lab (at ≈18 °C) until gill resorption was complete. I considered this the terminus of metamorphosis, and at this point I recorded the date and live mass to the nearest 0.001 g using an electronic top-loading balance. I used four different treatments (hydroperiods) in the experiment, drying the tanks in 50 d, 75 d, or 100 d from the addition of the fi rst hatchlings. In the last treatment, the water level remained constant. Each treatment was replicated four times for a total 16 tanks. The ponds were drained according to the same gradual drying curve modeled on natural, ephemeral wetlands by lowering the standpipe every other day. The date drying was initiated and completed varied among the three drying treatments. The 50-d treatment began drying 25 d sooner than the tanks in the 75-d treatment, which in turn began drying 25 d earlier than the tanks in the 100-d treatment. The daily rate of water loss once drying began was the same among the treatments (see Ryan and Winne 2001). On the last day of each hydroperiod (i.e., the day of complete drying), I searched through the leaf litter to collect any survivors. All individuals were sacrifi ced in a 10% alcohol solution and fi xed in 10% neutral buffered formalin. The experiment ended at day 160 when I drained the constant hydroperiod tanks and found no survivors, suggesting that the 160-d constant treatment was suffi cient to permit metamorphosis of all surviving individuals. Tank means were used as experimental units in all statistical analyses. Survival was calculated as the proportion of the original number of individuals (40) in each tank recovered at the end of the hydroperiod (regardless of metamorphic state). I compared survival across treatments with one-way analysis of variance (ANOVA), using the angularly transformed proportion to meet the assumptions of ANOVA. I used a multivariate ANOVA (MANOVA) to compare age and mass at metamorphosis and proportion of survivors completing metamorphosis as response variables for the 75-d, 100-d, and constant treatments; no individuals in the 50-d treatment completed metamorphosis, and thus these tanks were not included in the MANOVA. In order to meet the assumptions of parametric tests, I used the inverse-transformed days to complete metamorphosis (1/d), log-transformed mass, and angularly transformed proportion completing metamorphosis. Univariate ANOVAs were used to evaluate each response independently with α = 0.0125 to account for multiple 622 Northeastern Naturalist Vol. 14, No. 4 comparisons. In each univariate ANOVA, Tukey’s post-hoc tests were used to identify signifi cant differences among the treatments. Results Survival of larvae and juveniles to the end of the hydroperiod did not differ signifi cantly among the treatments (F3,12 = 1.51, P = 0.262; Fig. 1A). However, no individuals in the 50-d treatment completed metamorphosis prior to complete drying. The treatments had a signifi cant effect on metamorphosis (Wilks’ λ = 0.04459, F6,14 = 8.717, P < 0.001). This effect was due to difference in the completion of metamorphosis and age at metamorphosis. Figure 1. Mean (+1 SE) proportion of each treatment surviving to the end of the hydroperiod (A), and proportion of survivors completing metamorphosis by the end of the hydroperiod (B). Bars over treatments indicate no signifi cant differences. 2007 T.J. Ryan 623 The proportion of survivors completing metamorphosis varied signifi cantly among the remaining treatments (F2,9 = 18.44, P = 0.001), with metamorphic success increasing with longer hydroperiods (Fig. 1B). Unmetamorphosed individuals were relatively common in the 75- and 100-d hydroperiods (35% and 15% of survivors, respectively). The timing of metamorphosis was also infl uenced by hydroperiod. Metamorphosis was completed earlier in the 75-d treatment than the 100-d and constant treatments, and completed earlier in the 100 d treatments than in the constant treatment (F2,9 = 35.94, P < 0.0001; Fig. 2). At the completion of the 75-d hydroperiod, only 21.3% and 20.0% of hatchlings survived and completed metamorphosis in the 100-d and constant treatments, respectively (compared to 60.65% in the 75-d treatment). Only 51.9% of all larvae that would eventually complete metamorphosis in the constant treatment were done when the 100-d hydroperiod was completed. In all, 300 individuals completed metamorphosis; of the earliest 25% of successful metamorphs (n = 75), nearly half (n = 34) came from tanks in the 75-d treatment. Despite the strong effect on age at metamorphosis, there was no corresponding effect on the size at metamorphosis (F2,9 = 0.75, P = 0.498; Fig. 2). The 75-d treatment displayed considerably less variation in both age and size at metamorphosis as compared to the 100-d and constant treatments. Discussion Most previous data on the larval life history of Small-mouthed Salamanders are anecdotal (summarized in Petranka 1998) or potentially confounded with other factors. For example, Phillips et al. (2002) documented the sizes of metamorphic Small-mouthed Salamanders emerging from a natural wetland Figure 2. Mean (± 1 SE) age and size at metamorphosis (closed symbols; open symbols represent tank responses). The 75-d treatment is represented by diamonds, the 100-d treatment is represented by squares, and the constant treatment is represented by triangles. 624 Northeastern Naturalist Vol. 14, No. 4 in two consecutive years, fi nding that metamorphs were signifi cantly larger in a year with a longer hydroperiod. The difference in the hydroperiods in their study was only 10 d, but the difference in size was two-fold (about 17 mm versus 34 mm snout–vent length), suggesting factors other than hydroperiod played an important role (e.g., competition with polyploid congeners) during the two years of their study. Also, the timing of pond fi lling differed by more than three weeks in the two years in the Phillips et al. (2002) study, which may have had signifi cant infl uence on the development of the rest of the wetland community, including potential prey items. The length of the pond hydroperiod did not infl uence survival of larvae to the end of the treatments, but it did have a signifi cant effect on the completion of and age at metamorphosis. About 66% of larvae subjected to a 75-d hydroperiod and 85% of larvae experiencing a 100-d hydroperiod metamorphosed, whereas the shortest hydroperiod used in this experiment (50-d) was not suffi cient for the completion of metamorphosis of any individual. On a practical level, survival to the end of the hydroperiod while failing to complete metamorphosis is meaningless in terms of population viability. However, in the scope of this experiment, it is important because with the lack of a difference in survival between the treatments, it is clear that a longer hydroperiod permits a greater proportion of the population to complete metamorphosis. The fi rst metamorphs appeared after 64 d, consistent with previous observations of a minimum larval period of 2 mo (see Minton 2001, Petranka 1998). However, the average age at metamorphosis in the 75-d treatment was 71 d, indicating that about 2.5 mo is more representative of the minimum hydroperiod required for a relatively high rate of metamorphosis for a population of Small-mouthed Salamanders. In treatments with longer hydroperiods, the average age at metamorphosis was signifi cantly longer (13 and 24 d longer in the 100-d and constant treatments, respectively) and proportionally fewer individuals had completed metamorphosis in the longer hydroperiods treatments when compared to shorter hydroperiods. A positive correlation between length of hydroperiod and age at metamorphosis indicates that the Small-mouthed Salamander responds to shortened hydroperiods by accelerating metamorphosis. Despite the signifi cant effects on the timing and completion of metamorphosis in the current experiment, the size at metamorphosis was not signifi cantly infl uenced by hydroperiod treatments, although there was greater variation in both the age and size at metamorphosis with increasing length of hydroperiod. This outcome is contrary to an earlier experimental result reported by Petranka and Sih (1987). In their experiment, Petranka and Sih investigated the role of habitat stability in the timing of and size at metamorphosis in Kentucky populations of Small-mouthed Salamanders and a stream-breeding sister species, A. barbouri Kraus and Petranka (Streamside Salamander). They found no difference in the timing of and size at metamorphosis among Small-mouthed Salamander populations, but did fi nd that size and age at metamorphosis were positively correlated, with earlier metamorphs smaller than later metamorphs. This result is consistent with some expectations of the Wilbur-Collins optimality model (Harris 1999), namely, that larvae experiencing slow growth should metamorphose as soon as possible (and thus at a small size) to escape a 2007 T.J. Ryan 625 poor larval environment, whereas larvae growing at a rapid rate should delay metamorphosis to capitalize on the favorable growth opportunity. With several populations represented in their experiment, local adaptation to hydroperiod regimes may explain the Petranka and Sih (1987) result. Because I used mesocosms as the unit of analysis in my experiment, I am unable to determine whether such a positive association between size and time exists within a tank or population. In a subsequent mesocosm experiment, early metamorphs from a high-density treatment (80 larvae per tank) were notably smaller than later metamorphs from the same mesocosm (T.J. Ryan and C.A. Conner, unpubl. data). It may be that within a population, age and size at metamorphosis are positively or negatively correlated, but this relationship is absent among experimental populations in this study. That body size was not increased under longer hydroperiods in my experiment suggest that a delay in metamorphosis beyond ontogenetic or physiological minima is not necessarily for the purpose of increased fi tness via larger size at metamorphosis, as predicted by Wilbur and Collins (1973). Another optimality model, proposed by Werner (1986), places the timing of metamorphosis in the context of balancing the risk of mortality associated with the larval (aquatic) versus the transformed (terrestrial) environments. According to this model, metamorphosis is not delayed solely to increase body size, but to put off the transition to an environment that carries a higher likelihood of mortality. If this explains the delay in metamorphosis of Smallmouthed Salamanders in my experiment, we would predict that terrestrial mortality rates would be higher relative to the growth opportunities than in the aquatic environment. Unfortunately, there is a paucity of data regarding the post-metamorphic ecology of juvenile Small-mouthed Salamanders (Petranka 1998), and future studies will be needed to evaluate the absence of size differences among metamorphs of signifi cantly different ages. Experimental manipulations have been used to demonstrate the effects of hydroperiod on metamorphosis for many species (e.g., Brady and Griffi ths 2000, Parris 2000, Rowe and Dunson 1995). Increasingly, these data are necessary for understanding—and hopefully mitigating—the effects of anthropogenic change on species inhabiting temporary wetlands. The Small-mouthed Salamander is apparently capable of persisting in moderately developed (e.g., suburban) areas longer than most salamanders and many other amphibians (Minton 2001). Access to proper breeding habitats is a primary concern for the management of Small-mouthed Salamanders (Petranka 1998), as is the case with most other amphibians. Despite relatively robust populations throughout its range, there may be reason to be concerned for the long-term persistence of Small-mouthed Salamanders in regions where development (and thus habitat conversion) continues. Habitat conversion is one of the most conspicuous activities of human societies; approximately 50% of land surfaces globally have been converted to either agricultural or urban habitats (Chapin et al. 2000). Nearly 25 million ha of wetlands are estimated to have existed in the Midwest prior to European settlement; at present less than half of that area remains wetlands (Economic Research Service/USDA 1998). In Indiana, for example, of the estimated 626 Northeastern Naturalist Vol. 14, No. 4 more than 2 million ha of wetlands existing prior to western settlement (i.e., approximately 1780), only 15% remain at present (Indiana Wetlands, 2004). Prior to the 1980s, the primary reason behind wetlands loss in the USA was conversion to agricultural lands, but between 1982–1992, nearly 60% of wetland loss was due to urbanization. Small wetlands are used as nuptial/natal sites by a large number of amphibians, and there is limited protection for such wetlands under the most widely followed management guidelines (Semlitsch and Bodie 1998). Indeed, the 2001 US Supreme Court decision that reinterpreted the defi nition of “navigable waters” protected under the Clean Water Act (US Federal Register 68(10):1995–1998; 2003) has put isolated (i.e., those not connected to streams, rivers, or lakes) and ephemeral wetlands at even greater risk. Semlitsch (2003) has argued that the loss of small wetlands through habitat conversion is the primary threat to the persistence of pond-breeding amphibian populations in general, and I suggest this is true for the Small-mouthed Salamander in particular. For example, Amos Ditch, the source pond in the present study, is <1 ha, and the average size of 19 wetlands used by Small-mouthed Salamanders as breeding sites in Eagle Creek Park in 1998 (D. Van Deman, Eagle Creek Park, unpubl. data) is only 1.89 ha. Alterations of the natural hydroperiod of small wetlands like these due to development—especially alterations that reduce hydroperiod to less than 2.5 mo—could have a signifi cant negative impact on individual populations of Small-mouthed Salamanders. Constructed permanent wetlands intended to replace natural ephemeral ones are unlikely to be suffi cient for maintaining populations, especially considering that the Small-mouthed Salamander lacks effective anti-predator behavior with regard to fi sh (Sih et al. 2000) that are frequently stocked in constructed permanent wetlands. Even subtle changes in upland habitats surrounding breeding ponds may also threaten the stability of populations through the effects on postmetamorphic survival and recruitment (Gray et al. 2004, Taylor et al. 2006). The loss of small, temporary wetlands is likely to affect not only individual populations, but metapopulation structure as well (Biek et al. 2002, Semlitsch 2003). The mean dispersal distance of adult Small-mouthed Salamanders is less than 60 m (Williams 1973). The loss of functional wetlands (i.e., those with hydroperiods conducive to successful Small-mouthed Salamander breeding and metamorphosis) across the landscape, even on a fairly fi ne scale, could result in decreased movement between breeding sites, and thus a reduction in the likelihood of recolonization following reproductive failure at a particular wetland. 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