Conservation of Western Pond Turtles (Actinemys. marmorata) on the Lower American River

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1 Conservation of Western Pond Turtles (Actinemys marmorata) on the Lower American River Milo William Kovet Sr. ENVS 190; Senior Thesis California State University, Sacramento November 14,

2 Table of Contents: Abstract pg. 3 Introduction.pg. 4 Study Area.....pg. 4 Background. pg. 6 Classification. pg. 6 Description pg. 7 Diet pg. 9 Habitat. pg. 9 Aquatic Habitat. pg. 9 Basking.pg.11 Terrestrial Habitat....pg. 13 Overwintering.....pg. 13 Nesting.....pg. 14 Clutch Size pg. 15 Survival and Recruitment.pg. 16 Predators..pg. 16 Hatchling Survival...pg. 17 Other Threats.pg. 19 Habitat Loss. pg. 19 Disease. pg. 19 Road Mortality. pg. 20 Invasive species...pg. 20 Recreational disturbance..pg. 22 Climate Change pg.23 Conservation Status... pg. 24 Methods..pg. 26 Visual Encounter Surveys......pg. 26 Results. pg. 28 Discussion...pg. 29 Conclusion..pg. 31 Figures....pg. 33 Literature Cited. pg. 40 2

3 Abstract Western pond turtles (Actinemys marmorata) (WPT) are found along the western coast of North America. The western pond turtle is the only remaining freshwater turtle species native to California. The western pond turtle faces increasing pressure from habitat loss due to urban and agricultural development of wetland ecosystems. Habitat degradation and persistent drought, in combination with competition with invasive species, has reduced the population of western pond turtles. Western pond turtle populations have declined in abundance in parts of their range due to lack of juvenile recruitment, a result of elevated nest and hatchling predation (Rosenburg et al. 2013). The western pond turtle is now listed by the California Department of Fish and Wildlife as a species of concern in California (Jennings et al. 1994). The Stevens Laboratory has been working to restore crucial habitat for western pond turtles along the lower American River. The western pond turtle study at Bushy Lake has begun preliminary research, monitoring the health and recruitment of western pond turtles. 3

4 I. INTRODUCTION Study Area In 1976 the California legislature passed the Bushy Lake Preservation Act. This was done in part by local organizations such as The Save The American River Foundation (SARA) that rallied to save the land from development by Cal-Expo and the City of Sacramento, who had plans to turn the area into a golf course. Instead of a golf course, the land was set aside as a nature preserve. In section 1 #5832 (C) of the legislation the United States Fish and Wildlife Service determined that this riparian habitat is of vital importance and an integral part of the American River (Section 5832 of the Public Resources Code). Since that time, 1976, bike trails have been built and signs have been put up explaining the importance of the riparian corridor on the lower American River. The land is currently owned by Cal Expo and managed by Sacramento County parks, however little if any restoration work had been done until Bushy Lake is a small lake located in the American River Parkway at N, W in Sacramento County, California (Fig. 1). The area consists of a riparian habitat along the American River and the adjacent flood plain. Bushy Lake is approximately 700 meters from the American River. During very large precipitation events, such as in 2016, the American River floods its banks and covers the entire space, connecting into Bushy Lake. The Bushy lake preservation area is home to a wide variety of flora and fauna. Native trees and shrubs such as the blue elderberry (Sambucus nigra ssp. caerulea), cottonwood trees (Populus fremontii), and many other species are found at Bushy Lake. The animals in the study area include a wide variety of native and non- native animal species including western pond turtles (Actinemys marmorata), red eared sliders (Trachemys scripta elegans), river otters (Lontra canadensis), crayfish, and numerous other species, including many birds such as great blue 4

5 herons (Ardea herodias), numerous waterfowls, and raptors such as red-shouldered hawks (Buteo lineatus). Western pond turtles (Actinemys marmorata) have been observed at Bushy Lake by researchers. Western pond turtles are either endangered or threatened throughout their range which extends from southern Washington down to Baja California (Fig. 1) (Bury et al. 2008). In California, western pond turtles are a species of concern (Jennings et al. 1994; Bury et al. 2008). The lower American River parkway is among the last remaining strongholds for western pond turtles along the American River, making it a key area for conservation and management efforts. This habitat has been going through the process of adaptive restoration by the Stevens lab. A monitoring study was setup and the adaptive management of the western pond turtle population was included in the overarching restoration plan at Bushy Lake. The adaptive management of the western pond turtle population at Bushy Lake started in We began doing visual encounter surveys with binoculars and it appeared that most of the turtle population consisted of western pond turtles. It became apparent that there was another species of turtle in the restoration site, the invasive species of turtle known as the red eared slider (Trachemys scripta elegans). My initial hypothesis was that there were more western pond turtles than red eared sliders at Bushy Lake. It was hypothesized that recruitment of hatchling turtles into the population may be low due to no visual encounters with small turtles being recorded. Only after a full year of visual encounter surveys and monitoring did researchers find small juvenile turtles, though only very rarely have they been scene. No nesting location have been found, making the recruitment of hatchlings into the Bushy Lake population unknown. 5

6 However, later in the study the initial hypothesis was rejected as it was discovered that most of the turtle population consisted of red eared sliders based on further visual encounter surveys. In 2018, my hypothesis was that the western pond turtles have been pushed to the fringes of the available habitat and are being outcompeted by the red eared sliders, and, that recruitment of juvenile turtles into the population is still very low. In 2018 more evidence of recruitment was found, yet it has been difficult to identify the juvenile turtles to the species level based on visual encounters. Many unanswered questions about the ecology of the western pond turtles at Bushy Lake remain. The site itself is a crucial refugia, the last along the lower stretches of the American River, the western turtle population found here are extremely important to the conservation of the species (Fig. 2). The Stevens lab plans on conducting further studies in the spring of 2019 with the hopes of starting a mark and recapture program that will help to calibrate the visual encounter survey data already recorded. Lack of juvenile recruitment due to elevated nest and hatchling predation has been cited as the largest reason for the decline of the western pond turtle and researchers are working to locate nesting sites and protect them from predation. Through continued experimentation and adaptive management, researchers hope to conserve the western pond turtles found at Bushy Lake. Background Classification There has been somewhat recent discrepancy on the classification of the western pond turtle. The species has been classified as Actinemys marmorata based on genetic and taxonomic analysis (Bury et al. 2008). Previously the western pond turtle was classified as Clemmys marmorata or as Emys marmorata with the hypothesis that two distinct subspecies existed 6

7 (marmorata marmorata and marmorata pallida) (Holland 1994). This was based on morphological differentiation, yet, when DNA analysis was done to confirm the populations genetic variation it was concluded that the western pond turtle comprises four genetically and geographically distinct clades rather than two subspecies (Spinks et al. 2005). Description The western pond turtle is a medium sized semiaquatic freshwater turtle that has a broad, smooth carapace that usually reaches a maximum length of 8 inches (Rosenberg et al. 2013). The carapace color tends to be drab olive and reticulated, and the plastron is generally a light yellow. Males usually have varying degrees of pale yellow on the neck and chin, but otherwise the turtle s skin is gray to almost black and is often mottled (Rosenberg et al. 2013) (Fig. 3). The male western pond turtles have a concave plastron whereas the female s plastron is generally flat (Fig. 4). The thickness of the tail is also markedly greater in males. Juveniles tend to have mottling on the throat and their limbs are striped with yellow rather than mottled (Rosenberg et al. 2013). The western pond turtle (Actinemys marmorata) (WPT) is very small when it hatches, around the size of a quarter (Rosenburg et al. 2013). Research on nest and hatchling survival is the highest research priority because these stages in the life-cycle have not received attention due to the difficulty in their study (Rosenberg et al. 2013). Western Pond Turtles exhibit facultative emergence, they hatch either in the spring or later in the fall (Rosenburg et al. 2013). Western pond turtles are the only turtle species known to spend an extended duration of time around their nests after hatching. The baby western pond turtles dig their way out of their nests and remain within 2 meters of the nest chamber for an extended period (Rosenburg et al. 2013). The hatchlings remain either in the nest or near the nest due to a behavioral response to minimize the 7

8 energy demands of trying to move to a water source during adverse weather conditions (Rosenburg et al. 2013). Mortality due to dehydration has been observed, necessitating the need for hatchling turtles to move and find water after leaving the nest, or to bromate (Rosenburg et al. 2013). Emergence behavior of western pond turtles has been found to be synchronized, with many different clutches hatching at the same time (Rosenburg et al. 2013). Western pond turtles show substantial individual variation in the timing that they permanently leave the nesting site (Rosenburg et al. 2013). One study used radio transmitters on the hatchlings and observed one of the turtles staying in the nest for 20 days after its siblings had departed (Rosenburg et al. 2013). Western pond turtle hatchlings show high asynchrony, with some individuals staying near the nest for up to 2 months after their siblings have departed. (Haegen et al. 2009). Being so small when first hatching means that the western pond turtle is prey to a wide variety of predators. Leaving the nest at different times, the asynchrony, is hypothesized as a way for the western pond turtle to hedge its bets against things such as predation and thermal stress (Haegen et al. 2009). The western pond turtle has adapted to predation by being cryptic. The hatchling western pond turtles are rarely seen in their natural environments (Haegen et al. 2009). Depending on the time of year the western pond turtle hatches they may not go straight for a water source. Hatchlings that emerge in the fall are more likely to either stay in the nest cavity for an increased duration, or head for the surrounding terrestrial habitat to bromate (Haegen et al. 2009). Hatchling western pond turtles that remain out of the water create small depressions called forms where they are completely covered. The hatchling turtles embed themselves in soil or under duff and remain in these forms for an extended duration, some up to 22 days (Rosenburg et al. 2013). 8

9 Diet Western pond turtles are omnivorous and opportunistic feeders. They forage exclusively in aquatic habitats and do not eat or drink when they are bromating on terrestrial habitats (Haegen et al. 2009). The diet of hatchling western pond turtles is mainly carnivorous, including larvae of aquatic insects, earthworms, mollusks, and crustaceans. As they mature the western pond turtle preys on vertebrates such as tadpoles, frogs, and small fish. When they are young the western pond turtles eat whatever insects and invertebrates they can catch (Rosenburg et al. 2013). As they grow older the western pond turtles incorporate a wider variety of plants into their diet, yet they remain opportunistic feeders (Rosenberg et al. 2013). Adult western pond turtles eat aquatic plants and aquatic roots, making up some of their diet. However, western pond turtles have been known to scavenge, eating dead waterfowl and fish, another indication of the extent of their opportunistic feeding habits (Rosenberg et al. 2013). By being omnivorous and opportunistic the western pond turtle can adapt to a wide variety of aquatic habitats. Habitat Aquatic habitat Western pond turtles are found in both permanent and ephemeral aquatic habitats ranging from southern Washington down to Baja California (Fig. 2) (Rosenburg et al. 2013). They prefer either stagnant or slow-moving water bodies. Western pond turtles inhabit a broad range of aquatic habitats including sloughs, streams, large rivers, human-made ponds (including flooded gravel pits), irrigation canals, small lakes, reservoirs, marshes, oxbow lakes formed from larger rivers and even sewage treatment ponds (Rosenberg et al. 2013, Germano 2010, Winchell et al. 2016). When found in streams the western pond turtle prefers slow moving water and very deep pools which they dive into to escape predation (Rosenburg et al. 2013). 9

10 The microhabitats found within the main bodies of water that are suitable for western pond turtles include adequate woody debris for basking, pools, and ponds with muddy bottoms. Underwater refugia is critical for western pond turtles (Rosenburg et al. 2013). They use undercut banks and submerged large woody debris to escape predation from river otters and mink (Rosenburg et al. 2013). The western pond turtle prefers habitat with open banks, tree stumps, logs, and any other large objects that they can crawl up onto and bask on (Rosenburg et al. 2013). When basking the western pond turtle is ever alert for predators and will choose habitat that provides adequate refugia in the form of thick brush or trees behind, and open water in front. When found in large lakes and reservoirs western pond turtles seek the protection of coves, preferring southern exposure with shallow water (Rosenburg et al. 2013). There may be a correlation between having high density of emergent vegetation that contributes to a high density of invertebrate prey, and the resulting ecosystems can support more western pond turtles, yet more research needs to be done to confirm this (Rosenburg et al. 2013). The aquatic environment is very important to western pond turtles, however, there has been considerably less research on aquatic than on terrestrial habitat selection (Reese et al. 1997). This remains an important research area and presents opportunities for adaptive management as further studies are conducted. Hatchling western pond turtles need aquatic habitat with warm, slow moving water and extensive emergent vegetation (Rosenburg et al. 2013). Hatchlings, during their first month, move very short distances. Telemetry studies have found the maximum daily movement of hatchlings was only 5.8 meters (Rosenburg et al. 2013). During a three-week timespan, these hatchlings remained hidden under mud and vegetation for the entire time (Rosenburg et al. 2013). Hatchlings have been found in small ephemeral water bodies. One hatchling western 10

11 pond turtle was basking on a small piece of vegetation in a puddle only 2.5 cm deep, and another was found in a cow hoof-print that was embedded in a wetland (Rosenburg et al. 2013). Bushy Lake provides this type of habitat for western pond turtles. The lake itself is fed by ground water pumped from Cal-Expo and can be potentially kept full of water even in the summer months. The bottom of the lake is muddy, as discovered by researchers in 2016 when the water level was low due the extreme drought conditions. There is adequate emergent vegetation and microtopography that provides ideal habitat for hatchling western pond turtles (Rosenburg et al. 2013). There are deep pools and numerous banks and submerged logs that provide underwater refugia from predation for western pond turtles. Bushy Lake has many cottonwood trees (Populus fremontii) that provide large woody debris for basking locations. Basking Basking is a method of raising and maintaining body temperature and is a prominent behavior of the western pond turtle (Rosenburg et al. 2013). Western pond turtles spend most their active life in water (Boyer 1965). This is where western pond turtles eat and drink, they fast when bromating up on terrestrial habitats (Boyer 1965). Basking is very important since this is when all the metabolic processes associated with consuming food happen, which must be done with a consistent body temperature (Boyer 1965). Just about any object protruding from the water that can be climbed upon is potentially suitable basking material (Alvarez 2005). Western pond turtles will share basking sites and may even seek out basking sites already in use by other turtles (Rosenburg et al. 2013). An otherwise suitable habitat may become unsuitable for western pond turtles if there are not adequate basking sites available (Rosenburg et al. 2013). When they are basking the western pond turtles will flee into the water at the slightest 11

12 disturbance. Repeated disturbance of basking turtles will reduce habitat suitability and may result in a threat to the conservation of the species (Rosenburg et al. 2013). Basking is a key point in the competition between western pond turtles and red eared sliders (Boyer 1965; Lambert et al. 2013). Basking turtles compete for the best basking sites and are known to aggressively chase away smaller turtles if space runs out (Lambert et al. 2013). The two turtles competing will face off and engage in what is known as the open mouth gesture, with both opening their jaws very wide and performing a sort of joust that leads to the smaller turtle backing away and abandoning the basking site (Lindeman 1999). Since red eared sliders are larger (12 inches compared to 8) and more aggressive, they control the best basking sites when the two species compete for the same habitat (Lindeman 1999; Gibbs 2017; Lambert et al. 2018). Furthermore, experimental studies have been conducted that removed red eared sliders from a waterway and then observed the reaction of the western pond turtles to the new basking space availability (Lambert et al. 2018). This study found that after removing the red eared sliders the western pond turtles did not move into the new territory, and instead, stayed at the same basking sites already in use (Lambert et al. 2018). This study was only conducted over the course of a year and sited that more time would be needed to assess the long-term abandonment of key basking locations by western pond turtles after being outcompeted for them (Lambert et al. 2018). Bushy Lake has numerous basking sites that represent crucial habitat for western pond turtles. There are varying degrees of water depth and emergent vegetation found at Bushy Lake that provide habitat for western pond turtles of all ages and size classes. This is important for recruitment since hatchling western pond turtles require shallow water with plenty of emergent vegetation while adults prefer the safety of deeper pools and secluded basking sites. Western 12

13 pond turtles have a high site fidelity to the basking sites they use and will return day after day to a suitable location to bask on the same log (Lambert et al. 2018). Terrestrial habitat Overwintering Western pond turtles are opportunistic in selecting their overwintering sites (Reese et al 1997). If the aquatic habitat has a suitable muddy bottom, then the western pond turtles will overwinter in the mud. Telemetry studies have found western pond turtles overwintering under banks along streams, or buried under the duff of the forest floor, usually with 5-10cm of leaf letter covering them (Reese et al. 1997). There is a wide variance among the behaviors associated with overwintering and some western pond turtles have been known to come out of terrestrial refugia and bask, while others move around from site to site during the winter (Reese et al. 1997). Most western pond turtles spend a considerable amount of time on land during the winter. The western pond turtles bask, nest, disperse and bromate during the winter (Reese et al. 1997). This behavior is highly dependent on the habitat and climate of the ecosystem. For instance, western pond turtles in the Trinity River of northern California occupied upland terrestrial habitats for seven or more months of the year, with much of the time spent at overwintering refugia (Reese et al. 1997). The timing of the move out of water and on to the land correlates with the changing of rainfall patterns and the seasons for western pond turtles (Zaragoza et al. 2015). Western pond turtles use terrestrial refugia primarily during late fall to early spring, but they have been observed to also use this habitat during summer if their ephemeral aquatic habitat dries up (Zaragoza et al. 2015). This is especially true for Mediterranean climates such as California 13

14 where streams and rivers are reduced to trickles by August leaving the turtles with no aquatic refugia (Reese et al. 1997). In the coastal creeks and lagoons of California researchers found that all twelve of the radio-equipped western pond turtles being tracked left the river for overwintering sites between September and December (Rathbun et al. 2002). Turtles returned to the aquatic habitats beginning in February and continuing through June (Rathbun et al. 2002). In one study movement to terrestrial overwintering sites started as early as late July through mid- December, yet most movement to upland sites occurred during September and October (Zaragoza et al. 2015). Bushy Lake provides essential terrestrial overwintering sites for western pond turtles. This habitat provides a broad array of vegetation structure necessary for western pond turtles including; forests, open grasslands, and shrubs (Zaragoza et al. 2015). Based on previous telemetry studies, some level of solar radiation is important during overwintering and plays a part in the selection of the sites (Reese et al. 1997). Studies have found that western pond turtles selection of overwintering sites were associated with less than 10% slope, good solar exposure, open ground cover and duff. Western pond turtles seemed to avoid dense grass and dense forest cover, possibly since too much cover blocks solar radiation (Reese et al. 1997). Nesting The western pond turtle is dependent on having suitable terrestrial habitat for nesting (Rathbun et al. 2002). Ideal nesting habitat is found in areas with little vegetation, usually consisting of grass and forbs (Rathbun et al. 2002). The soil requirements are compact soil composed of clay or silt, sandy loam alluvial deposits, and sometimes gravel mixed with soil. The nesting habitat is characterized by having a high level of solar radiation exposure, in the open with no tree canopy to shade out the site (Rathbun et al. 2002). 14

15 Detailed nest evaluation studies have been conducted in southwest Washington using telemetry to locate the nests (Gonzales et al. 2008). These studies found that 26 of 29 turtles tracked nested within meters of permanent water, with the remaining 3 turtles found nesting meters away from the water source (Gonzales et al. 2008). Since western pond turtles occupy such a diverse range nesting sites often vary. However, most nest sites are near the turtles aquatic habitat, almost all nests occur within 200 meters of the water (Rathbun et al. 2002, Gonzales et al. 2008). The nesting habitat is adequate at Bushy Lake for western pond turtles. There is plenty of open space in the form of fields that stretch over 800 meters until they reach the American River that provide nesting locations with plenty of sun exposure and less than 10% slope. The riparian trees, mainly cottonwoods and willow species, provide a duff layer of leaves and overwintering habitat for western pond turtles. Clutch size The female body size of the western pond turtle and the amount of eggs she can produce has a very high correlation Gonzales et al. 2008). Western pond turtles can have clutch sizes ranging from a single egg, to over a dozen (Holland 1994). Male western pond turtles are sexually mature by 5-9 years and females at 7-10 years (Bury et al. 2008). The female western pond turtle has her first clutch of eggs when she has reached a carapace length of around 5 inches (Holland 1994). There is a correlation between the environment and the female western pond turtles reaching sexual maturity (Holland 1994). In the southern parts of the female western pond turtles range the females are sexually mature at around only 6-7 years old, yet further north and up into Oregon and Washington past the Rogue River the smallest gravid females are years old with a carapace over 5 inches (Holland 1994). 15

16 There is evidence after examination of over 1,200 gravid female turtles that this correlation of latitude and sexual maturity is connected to how many times per year females lay eggs (Holland 1994). In the southern reaches of the western pond turtles range the females tend to lay eggs each year and may double clutch. Yet, in the northern range and up into southern Washington there is evidence that most western pond turtles oviposit in alternate years (Holland 1994). The western pond turtle eggs are a creamy white in coloration and measure roughly 31-38mm in length and 20-24mm in diameter and weigh 8-10 grams. Incubation time for western pond turtle eggs is between days in California and hatching rate is around 70%. Complete failure of clutches is not uncommon for western pond turtles (Holland 1994). The hatchlings are tiny and measure only 25-30mm, 1 inch long. Since it has been hypothesized that the decline of the western pond turtle in its range may be either directly or indirectly correlated to nesting ecology it is important for conservationist to locate nesting sites and attempt to secure the nests from predation (Alverez 2014). This can be done by placing a fine mesh wire cage over the nesting site that would help to inhibit predation (Alvarez 2018). However, even a caged nest may be susceptible to predation. Studies of caged nests have found that some clutches are still preyed upon by unknown tunneling predators that circumnavigate the cage by tunneling straight into the nest and eating the clutch (Alvarez 2014). Survival and Recruitment Predators Adult western pond turtles are protected from most predators by their shell and their ability to dive into water and hide using underwater refugia (Bury et al. 2008). Yet, despite the protection afforded by their shell adult western pond turtles are still preyed upon by predators 16

17 such as river otters (mustelid spp.) The main predation threats from non-aquatic species come during overwintering times when the western pond turtle is up in its terrestrial habitat. During these vulnerable months western pond turtles are preyed upon by predators such as coyotes and other canids and even black bears. Several different predators take western pond turtles, especially juveniles and hatchlings. These include, yet are not limited to: the great blue heron (Ardea herodias), largemouth bass (Micropterus salmoides), bullfrog (Rana catesbeiana), osprey (Pandion haliaetus), bald eagle (Haliaeetus leucocephalus), raccoon (Procyon latar), grey fox (Urocyon cineroargenteus), coyote (Canis Zatrans), feral and domestic dogs (Canis familiaris), black bear (Euarctos americanus), river otter (Lutra canadensis), and mink (Mustela vison) (Holland 1994). Hatchling Survival The survival rate of western pond turtle hatchlings is very low, with mortality ranging from 80-94% (Bury et al. 2008). There are not many studies that have data on this subject as most will use the preferred method of head starting programs to ensure the viability of young western pond turtles in the wild due to the predominant view that post-emergence mortality is a conservation threat for the species (Holland 1994, Haegen et al. 2009). Population declines of western pond turtles have been attributed to predation by bullfrogs, smallmouth and largemouth bass (Holland 1994). However, a study in 2008 could not find definitive evidence of predation by these predators. It is still unknown to what extent bullfrogs and predatory fish play on the survival of hatchling western pond turtles (Bury et al. 2008). Great blue herons (Ardea Herodias) have been documented eating juvenile western pond turtles and are considered an important predator (Bury et al. 2008). 17

18 Lack of juvenile recruitment due to elevated nest and hatchling predation has been cited as the largest reason for the decline of the western pond turtle (Reese et al. 1997; Haegen et al. 2009; Rosenburg et al. 2013). There are a greater abundance of raccoons and skunks in urban areas than would have been present historically, making nest predation higher (Rosenburg et al. 2013). Despite this, there has been little quantification of these threats other than documentation that they are indeed some of the most common nest predators (Alvarez 2016). Reducing nest predation has been a major focus of management activities for western pond turtles and continues to be a focal conservation strategy (Alvarez 2016). Several land-management agencies have protected nests from predators by installation of enclosures, cages or other blockades that reduce egg stealing predators from accessing the nests (Alvarez 2016). The survival rates for adult western pond turtles are much higher than that of juveniles. Few studies have been conducted on the survival of adult western pond turtles since most of the conservation attention is focused on recruitment and protecting hatchlings (Rosenburg et al. 2013). The data that has been collected shows an 86-97% survival rate of adult western pond turtles. A four-year head starting study conducted in Washington found that out of 68 western pond turtles 6 died, with 5 of these deaths occurring during overwintering in upland habitat. At least four out of the six deaths were attributed to predation (Haegen et al. 2009). Lack of juvenile recruitment due to elevated nest and hatchling predation at Bushy Lake are major concerns. Researchers have been unable to locate the nests of turtles while monitoring the site. Due to the high urbanization of the surrounding area the population denisty of racoons and skunks are elevated (Rosenburg et al. 2013). Raccoons and skunks are nest predators that have been known to enact a significant level of predation on western pond turtles nests (Alvarez 2016). Assessment of whether predation pressure on nests is affecting population viability is a 18

19 major factor that should be considered when evaluating the best allocation of resources among different management options at Bushy Lake (Rosenburg et al. 2013). Other threats Habitat loss The life history of the western pond turtle places it in great danger of anthropogenic habitat destruction since the turtles need the availability of slow-moving water with deep pools in conjunction with terrestrial habitat suitable for both overwintering and nesting. Western pond turtles depend on oxbow lakes and wetland habitats. Loss of aquatic habitat has been substantial throughout the western pond turtles range (Holland 1994). Large amounts of aquatic and adjacent terrestrial habitat have been lost since major development of flood control has been implemented throughout many parts of the range of western pond turtles, especially in California. However, the western pond turtle is highly adaptable since it is an opportunistic feeder and can occupy many disturbed environments (Germano 2010). Having a high level of tenacity makes conservation of western pond turtles possible through much of their range. Despite this, habitat loss and habitat fragmentation are still major threats to the species and the allocation of suitable habitat will play a major role in conservation of western pond turtles in the future. Loss of terrestrial habitat is also due to land use zoning and planning regulations. Aquatic habitats have more protection under state and federal laws; upland habitats are more subject to development pressure and conversion to other uses. Sunny, well-drained soils upslope from rivers and creeks that are suitable nesting and overwinter areas for western pond turtles continue to be impacted by residential and agricultural development (Holland 1994). 19

20 Disease Disease is a major threat and has been known to kill entire populations of western pond turtles. Parasites have already been documented on western pond turtles at Bushy Lake restoration site, in the form of leeches (Fig 5). Nematodes are another parasitic threat to western pond turtles. Pathogens are a concern; a dead turtle was found on the banks of Bushy Lake, which may have been killed by disease (Fig 6). The invasive turtles, red eared sliders (Trachemys scripta elegans) are often bred in unsanitary conditions in which they are housed with other turtle species, making the risk of cross contamination likely (Holland 1994). An outbreak of upper respiratory disease killed 40% of a western pond turtle population in Washington in one documented case. Then, another 42 dead western pond turtles were found in a pond in Northern California with episodic disease was ruled as the killing agent. Road mortality Adult female western pond turtles are known to travel as far as 400 meters when searching for a suitable nesting site (Reese et al. 1997; Haegen et al. 2009). Traveling long distances across terrestrial habitats is by itself one of the leading causes of mortality for adult western pond turtles as they are easily preyed upon during this time (Reese et al. 1997; Haegen et al. 2009). Road mortality is especially dangerous for female western pond turtles since they travel far distances from water looking for suitable nesting habitat. Being run over has been estimated to be a cause of 3-5% of the total western pond turtle mortality rate in some studies (Holland 1994). Due to the way roads often bisect nesting habitat near streams, western pond turtles are forced to cross roads to reach suitable nesting habitat. Road mortality, and the resulting reduced connectivity between aquatic and upland habitats, is likely to increase as a threat to western pond turtles as human populations grow and more roads are built. 20

21 Bushy Lake is bisected by roads used by county officials and local power companies. These people have reported seeing turtles while driving down by the Bushy Lake, though road mortality has not been observed. The hacked up part of a shell of a red eared slider was recently discovered along a gravel path that had apparently been run over by a large mower, however. The amount of mountain bikes on the trails around Bushy Lake is a concern for juvenile and hatchling western pond turtles and further necessitates locating the nests and placing warning signs to educate the public. Invasive species The pet trade also threatens native freshwater turtles. Pet stores sell a variety of nonnative turtles, the most popular being the red eared slider (Trachemys scripta elegans). The release of non-native pet turtles into natural areas has caused an explosive growth of red eared sliders in many of the urban waterways in the western pond turtle s range (Spinks et al. 2003). This increases competition for limited resources and introduces diseases to native turtles (Spinks et al. 2003; Thompson et al. 2010). The threat posed by introduced turtle species is growing. It has been documented that once a population of a successful invasive species has become established in an ecosystem they are nearly impossible to remove and may require years of adaptive management (Thomson et al. 2010). The number of new releases of red eared sliders into the wild is presumably increasing. Given access to western pond turtle habitat from urban growth and increased access to recreational areas has led researchers to study the competition between red eared sliders and western pond turtles in recent years, though no definitive study has been published (Patterson 2006, Gibbs 2017). Oregon has recognized this threat by red eared sliders and classified the species as Nonnative Prohibited Wildlife by Oregon state law (OAR ) (Rosenburg et al. 21

22 2013). California and Washington have not made red eared sliders illegal in the pet trade and they are still commonly found in pet stores (personal reference). California has passed laws making the consumption of the turtle illegal due to the high correlation between them and dangerous bacteria such as salmonella (Harris 2010). Red eared sliders can lay six clutches of eggs a year with each clutch having as many as thirty eggs (Gibbs unpublished). In comparison to the single to a dozen eggs of the western pond turtle, who only oviposit twice a year at the most, it becomes easier to understand how the population boom of red eared sliders occurs. Beyond even this, the red eared sliders can begin breeding at only three years of age (Gibbs unpublished). The western pond turtle takes six years on average to reach breeding age (Patterson 2006). This may explain the observations made by researchers who have observed explosive growth rates of red eared sliders after initial periods of stability (Thompson et al. 2010). Other invasive species include the bullfrog and species of large fish such as bass. While it is still unknown what the impacts of these predators have on the populations of western pond turtles it is important to take them into consideration when attempting to conserve the species. Head starting programs are successful ways to circumnavigate loss of hatchlings to predation and are an important conservation strategy (Reese et al. 1997, Haegen et al. 2009). Recreational disturbance Western pond turtles are very sensitive to disturbance when basking and nesting. In sites with heavy disturbance the western pond turtle s ability to thermoregulate may be negatively impacted. This is a serious threat since thermoregulation from basking is essential for digestion and other metabolic processes (Rosenburg et al. 2013). Many riparian areas in urban setting have extensive trail systems, either for walking or for bicycling. Emphasis should be placed on 22

23 not disturbing the native turtles at these locations. As an example, at Bushy Lake restoration site the land owners Cal-Expo have placed signs regulating bike riding through the restoration area. This can be expanded to include not disturbing western pond turtles and signs can be placed in strategic location known for having large numbers of basking turtles. The nesting locations are unknown at this site, yet once they are located warning signs would provide at least some protection from disturbance. Other recreational disturbances include fishing. At a site in Oregon 3.6% of the turtle population has marks or scars associated with recreational fishing activity (Rosenburg et al. 2013). However, in California it is legal to catch turtles with a fishing permit and a rod and reel (California Fish and Wildlife 2018). No fishing has been observed at Bushy Lake, yet with the high amount of homeless people in the vicinity fishing may still pose a threat (personnel observation). Bushy Lake has a population of homeless people who may be impacting the western pond turtle population. Trash has been found in the water and the banks of Bushy Lake, including hypodermic needles. A wildfire that impacted Bushy Lake in 2015 was attributed to the homeless population and campfires. Personal observations have not confirmed the homeless population at Bushy Lake to be a direct threat, yet disturbance while basking and other indirect influences of anthropogenic pressure on the western pond turtle population needs to be taken into consideration as part of the overall conservation plan. Climate Change Climate change has and will continue to cause major disturbances in environmental conditions for many organisms. For freshwater turtles in general, water temperature is likely a factor limiting distributions. Changing water temperature has the potential to cause large 23

24 changes to the distribution of turtles in California with cold water being a limiting factor in the reproductive success of the invasive red eared slider population (Rosenburg et al. 2013). Climate change will also likely affect hydrological patterns, which could also impact freshwater turtles considerably. Drought is a major factor for western pond turtles in California and has been attributed to climate change in recent years, leading to increased western pond turtle mortality (Purcell et al. 2017). During the prolonged drought that affected California researchers found dried up ponds littered with many western pond turtle shells (Purcell et al. 2017). Climate change has the potential to change the distribution of suitable habitat for western pond turtles. The direct and indirect effects of climate change on freshwater turtles are important to consider, although predictions for effects are in their infancy (Purcell et al. 2017). In 2013 California Fish and Wildlife rescued a population of 61 western pond turtles from Lake Elizabeth in southern California (California Department of Fish and Wildlife 2018). Western pond turtles have been declining rapidly in southern California and this population of rescued western pond turtles represent an important genetic diversity component of the species. Lake Elizabeth was quickly drying up, and after the rescue three of the turtles died from thermal stress. The turtles were housed at a nearby facility at the University of Southern California Los Angeles in temporary tanks until Lake Elizabeth was again suitable habitat. As climate change and increasingly severe droughts continue to threaten western pond turtles in California adaptive management such as this will be crucial for the conservation of the species. Conservation Status The western pond turtle is considered a sensitive species and a species of conservation concern by most public agencies in California, including the California Department of Fish and Wildlife (California Department of Fish and Wildlife 2018). The western pond turtle is listed as 24

25 an endangered species in Washington state and a species of concern in Oregon (Bury et al. 2008). The IUCN Red List has the western pond turtle listed as vulnerable, though global assessments have not been conducted since 1996 (IUCN Red List 2018). This is primarily due to the considerable degradation and loss of wetland habitats within the extent of the western pond turtles range, and the presumed unsustainably high level of nest and hatchling predation (Bury et al. 2008). The vulnerability of western pond turtles is largely due to the numerous threats (listed above) that will increase as the human population of California increases. The assessment of the vulnerability of this species in California is partly dependent on understanding the level of connectivity among existing populations, whether recruitment of juveniles into breeding adults is enough for population viability, and how future modifications to the landscape in California will affect existing populations. The western pond turtles broad distribution, including occupancy of human modified environments and areas of high turtle density, provide many opportunities for effective management. Concern over the conservation of western pond turtles throughout their range prompted a petition to list the species under the Endangered Species Act. The petition was filed in 1992, although it was later denied by the U.S. Fish and Wildlife Service (USFWS 1993a). The U.S. Fish and Wildlife Service denied the petition for two major reasons, the broad distribution of western pond turtles in their native range and their apparent ability to survive and reproduce in many human-modified environments (Rosenburg et al. 2013). The USFWS (1993a) cited the lack of evidence supporting the listing petition s claims of broad-scale threats. Due to lack of studies on recruitment, the claim of lack of juvenile recruitment due to elevated nest and hatchling predation was not enough evidence for listing (USFWS 1993a) (ECOS 2018). Much of the rationale for denying the petition, including broad distribution, occurrence in human- 25

26 modified habitats, and lack of supporting data for hypothesized threats, remains unchanged over the last 26 years. This points out the critical need for studies to confirm the recruitment challenges faced by the species (Reese et al. 1997; Haegen et al. 2009; Purcell et al. 2017). However, all the evidence to date suggests that the decline of western pond turtles is occurring in all parts of its range with the turtle now listed as endangered in Washington (Bury et al. 2008). The western pond turtle remains vulnerable due to the many threats discussed. A long-lived species such as the western pond turtle that requires both aquatic and upland habitats, and that occupies areas that are quickly becoming urbanized, must be placed into conservation strategies before being listed as a federally endangered species becomes a reality (Bury et al. 2008). Methods Visual Encounter Surveys The methods used in this research have been visual encounter surveys (VES). Visual encounter surveys are based on consistent timed periods in which quick assessments of species occurrence (found/not found) and various population dynamics such as counts, recording size classes, species, and other relevant data such as weather and any anomalies are recorded. Visual encounter surveys have been used to identify and quantify turtle species at Bushy Lake since the Spring of 2016 and part of continued monitoring since These surveys are repeated frequently, usually twice a week. The visual encounter surveys are done at specific locations around Bushy Lake where previous observational data has identified basking turtles. These basking sites are tied to the western pond turtles high site fidelity and are important pieces of data for continued monitoring efforts (Lambert et al. 2018). The initial hypothesis was that there were far more western pond turtles than red eared sliders at Bushy Lake. The sampling sites for visual encounter surveys are at three main basking 26

27 sites around Bushy Lake (Fig. 1). This sampling area has a perimeter of 1.5 kilometers and a surface area of 4.31 hectares. Visual encounter surveys were carried out at each basking site beginning in February, with x10 binoculars and a x100 spotting scope. Visual encounter surveys were between 1 and 2 person-hours of effort depending on the number of turtles present on a given day. Between one and five observers would go together and the visual encounter surveys were conducted as a team. The observations were done systematically starting at the same sampling area and then slowly working around the lake to the far side. The visual encounter surveys were done in a single pass in order to avoid counting the same turtle twice. Visual encounter surveys were complete when all the habitat in the vicinity of Bushy Lake had been scanned. The visual encounter surveys at Bushy Lake recorded the number and the species of all turtles identified. Turtles were then divided into size classes with juveniles being anything under 4 inches in length, medium size turtles 4-6 inches and large turtles greater than 6 inches. The methodology of the size classes corresponds to the sexual maturity of western pond turtles who do not reach sexual maturity until larger than 5 inches and can grow as large as 8 inches. Since basking intensity varies with the time of day, time of year, and the ambient weather conditions, all this information is considered pertinent and was recorded. Any disturbances were recorded as well. Disturbances can be frequent at the study site since Bushy Lake is adjacent to Cal-Expo and the area itself is used for a wide variety of recreational and even military exercises. The relative abundance of red eared sliders (Trachemys scripta elegans) was used as a percentage of the total amount of turtles observed. The comparison between the amount of red eared sliders and western pond turtles (Actinemys marmorata) was a focus of data collection and extra time was spent differentiating the species of turtles for later quantification. Visual 27

28 encounter surveys have been shown to be accurate when compared to later mark and recapture data (Thompson et al. 2010). Separate visual encounter surveys were performed with the intent to find hatchling and juvenile turtles. The necessity for a separate survey for hatchlings is based on the difference of habitat occupied by the juveniles versus the adult western pond turtles (Haegan et al. 2009). Areas of thick emergent vegetation and warm shallow water were monitored for hatchling turtles. Monitoring for nesting sites was conducted during the known nesting season beginning in April and ending in June of The western pond turtle will often urinate prior to digging a nest and the wet ground can be used as a distinguishing factor of a newly dug nest (Alvarez 2018). Western pond turtles are known to travel as far as 400 meters from open water to dig a nest, therefore a wide area was searched that fit this perimeter. During surveys anything that resembled a hole in the ground was investigated by carefully removing the soil and examining the hole for eggs or signs of nesting behavior, including the remains of egg shells. Results The hypothesis that a high number of red eared sliders (Trachemys scripta elegans) at Bushy Lake in proportion to the amount of western pond turtles was verified by the data collected and accepted. Since the area is located adjacent to major metropolitan areas this is consistent with the results of other studies and confirms the hypothesis that anthropogenic release of red eared sliders is bolstering the population (Thomson et al. 2010). The original hypothesis that many of the turtles were western pond turtles was rejected pending further study that may include mark and recapture (see discussion). The percentage of red eared sliders found in Bushy Lake is 79% (10:2 turtles) based on visual encounter surveys (Fig. 7). This confirms 28

29 the second hypothesis that the red eared sliders are more numerous than the western pond turtles at Bushy Lake, yet this data needs to be calibrated with a mark and recapture study. The high count of turtles seen in a single day doing visual encounter surveys at Bushy Lake in the spring of 2018 was 64. More young and juvenile turtles were spotted in 2018 than 2017, though this was in part due to further exploration of the area into coves and small inlets searching for recruitment and small turtles outside of the visual encounter survey locations. The numbers of juvenile turtles observed is still very low. On a day when 58 turtles were observed only two of them were less than 4 inches. These results are consistent with the low amounts of juvenile turtles encountered in other studies and may represent the ongoing trend hypothesized in the literature that suggests recruitment is a major area of concern for the species (Reese et al. 1997; Haegen et al. 2009). The smallest turtles observed could not be identified to the species level based on how quickly they would vacate basking sites, making classification impossible without further efforts. Though mark and recapture has not started yet at Bushy Lake a couple of red eared sliders have been found and examined. When examining a turtle parasite load is checked for around the tail. Nest the shell is examined for shell rot or soft-shell diseases. Limbs are accounted for and the turtles respiratory condition is checked by examining the nostrils for any bubbles or mucus secretions. The red eared sliders seemed healthy in every respect except for parasites. Large leeches were found on both, though no nematodes were observed. Discussion As 2018 draws to a close many questions are left to be answered regarding all the turtles at Bushy Lake. The hypothesis that red eared sliders are more numerous than western pond turtles at Bushy Lake being accepted opens many questions about competition and diseases that 29

30 cannot be answered until spring when the turtles re-emerge from overwintering and mark and recapture commences. The spring of 2019 will be the beginning of the Stevens Lab s mark and recapture program, with the hopes of calibrating the visual encounter data and answering some of the mysteries surround the turtle populations. In conjunction to mark and recapture, researchers at Bushy Lake plan on installing wildlife cameras and artificial basking platforms to help quantify the population dynamics of Bushy Lake. Wildlife cameras will play an important role in quantifying the amount of recruitment by hopefully capturing the elusive hatchling turtle activity. One of the crucial elements to the conservation of western pond turtles mentioned repeatedly in the literature is recruitment. A population of long-lived species such as western pond turtles can appear viable, yet without recruitment the population is senescent and will not persist (Spinks et al. 2003). Lack of studies and empirical data to back up the hypothesis that this is a crucial conservation issue was one of the reasons the western pond turtle was denied listing status by the federal government of the United States back in Most of the studies done on recruitment used telemetry to locate the nests of the females. Researchers at Bushy Lake have repeatedly searched for western pond turtles nests during visual encounter surveys and have never found one to date. By using telemetry, the guess work can be removed from the process and female turtles can be tracked to their nests which can then be monitored and protected with the hopes of increasing recruitment. Telemetry will be a crucial step in the adaptive management of the western pond turtle population at Bushy Lake. After further data on the competition between the red eared sliders and the western pond turtles at Bushy Lake is collected, the red eared sliders may need to be removed. It is our philosophy to do no harm during restoration efforts, and a sanctuary has been preemptively 30

31 located that will take as many red eared sliders as necessary. This work will be adaptive management since the prolific red eared sliders will undoubtably have clutches of hatchlings incubating in the nearby terrestrial habitat, ready to take the places of their removed relatives. Yet, once the general nesting grounds are located finding the nests of red eared sliders is a very real possibility. Disease may be a greater threat than competition, with the ability to extirpate entire populations of turtles. Detailed examinations of every turtle captured during the mark and recapture phase will hopefully give new data on the health of both populations of turtles at Bushy Lake. Two red eared sliders have been found by me during monitoring, and both turtles had several large leeches around their tail areas. Nematodes were an unknown threat at the time and will be checked for in the future. Data from the recruitment found by tracking nests can then be used to justify a head starting program. As discussed, head starting has been shown to be an excellent way to circumnavigate the heavy predation during the first year of the western pond turtle s life when mortality rates have been as high as 95%. After the spring of 2019 many of these questions will hopefully be answered and the door will be open for Bushy Lake researchers to follow up on these questions and find new ones of their own. Conclusion The chordates are a charismatic clade and the western pond turtle is a particularly beautiful example. People love turtles. Public awareness of the western pond turtles decline can easily result in better protection for the species with just simple things like educating people to not release pet turtles into the wild. It is my hope that California will follow Oregon and pass a law outlawing the sale of known invasive species in the pet trade. It is very surprising that 31

32 California does not have a law like this in place already since many of the existing laws involving exotic pets in the state are very strict (see ferrets). Not many people know that only one endemic turtle species remains in California. As climate change and droughts get worse, someone needs to protect our turtles. It would be a great travesty if we lost our native turtle. It is with great honor that I personally have worked with the western pond turtles, and I hope to continue conservation work in the future. The heart of the soul, the keeper of life. The blessing of health and the island of our people. KEYA (Turtle) ~The Lakota People 32

33 Figures Figure 1: Bushy Lake Restoration Area. The yellow polygons represent known turtle basking habitats. 33

34 Figure 2: Distribution of the western pond turtle in North America. Red points are museum and literature occurrence records. Source: Bruce Bury and David Germano (2008) 34

35 Figure 3 Western Pond Turtle with Mottled Patterns on skin. This was a melanistic morph trapped out at Suisan Marsh when training with UC Davis. 35

36 Figure 4: Male Western Pond Turtle on the Right and female on the left. Notice the male has a thicker tail and concave plastron. Photo taken while training with UC Davis. 36

37 Figure 5: Leech removed from behind the tail of a red eared slider. Invasive turtles are a known vector for disease and parasites. Photo taken at Bushy Lake by Milo Kovet

38 Figure 6: Deceased red eared slider. Cause of death unknown, possibly disease or drought. Photo Milo Kovet