Current situation of the Sonoyta Mud ( sonoriense longifemorale) population at Agua Dulce RAMSAR site in El Pinacate Biosphere Reserve, Sonora, Mexico

July 2018

Reserva de la Biosfera El Pinacate y Gran Desierto de Altar

Miguel A. Grageda García.

Coordinator of Natural Resources Management.

Héctor Diego García Miranda.

Field Biologist ACKNOWLEDGMENTS

This effort was funded through the P16AC01282/ASDM-41--Support conservation actions for Quitobaquito and Rio Sonoyta, which is a collaboration of the Organ Pipe Cactus National Monument, -Sonora Desert Museum and Pinacate Biosphere Reserve starting in March 2016.

We want to thank to all the experts, volunteers and people involved in this project:

Dr. Peter Holm, Dr. Tyler Coleman, Marie Long, Catherine Bartlett, Lourdes Ortiz, Sait Juanes Márquez.

And a special acknowledgment to Raúl ‘Don Ruly’, owner of the Papalote Ranch and part of the Agua Dulce RAMSAR site for providing access to his land and supporting this project.

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INTRODUCTION The Sonoyta mud turtle (Kinosternon sonoriense longifemorale) is a subspecies endemic of the Sonoyta River in northwestern Sonora, Mexico and the Quitobaquito Springs in southern Arizona, United States. This subspecies was first described by Iverson in 1981 based on morphometric analysis of 19 shell measurements of specimens from Quitobaquito in Arizona and sites in the Rio Sonoyta basin in Sonora. Currently the Sonoyta mud turtle is classified as K.s. longifemorale (Iverson 1981), as one of two subspecies of Sonora mud turtle and is considered a valid taxon by the scientific community (Crother 2012) based on the morphometric analysis by Iverson (1981) and genetic work by Rosen (2003) and Rosen et al. (2006). Two genetic analyses support that this subspecies is a recognizable entity compared to the other currently recognized subspecies (K. s. sonoriense), although it is not strongly differentiated. The other subspecies, K. s. sonoriense, is commonly referred to as Sonora mud turtle. The currently accepted classification is: Kingdom: Animalia Phylum:Chordata Class:Reptilia Order: Testudines Family: Subfamily: Kinonsterninae Tribe: Kinosternini Species: Kinosternon sonoriense Subspecies: longifemorale Other subspecies of the species Kinosternon sonoriense are found in the southwestern U.S. and Sonora. Although individuals from all populations have adaptations necessary for inhabiting environments that dry periodically, behavioral and physiological responses to water stress vary among populations (Peterson and Stone, 2000; Lignon and Peterson, 2002). Mud movements vary with water availability at regional and local scales (Stone, 2001). The Sonoyta Mud Turtle is in the IUCN Red List of Threatened Species considered as ‘Near Threatened’ since 2011 (Van Dijk, 2011) and by the Mexican law NOM-059-SEMARNAT- 2010 as Endemic and in ‘Danger of Extinction’ (SEMARNAT 2010)

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STUDY SITE We studied Sonoyta Mud Turtles in the area known as Agua Dulce (Figure 1). It is a wetland designated as RAMSAR in February 2nd, 2018 (Ramsar, 2008; Ramsar, 2018). It is located within the Sonoyta River flow (31° 55’ 27’’ N, 113° 01’ 17’’ W), with a surface of 39 ha and an extension of 2 km. The Sonoyta river originates near the Pozo Verde mountain range in Sonora, Mexico. It flows to the west for 207 km, at this point it reaches the area known as Agua Dulce, and then keeps flowing south for 88 km until it reaches the Sea of Cortez. The streambed is formed by gravel, bedrock and sand. Vegetation bordering the river is dominated mainly by the invasive salt cedar (Tamarix ramosissima) with presence of mesquite (Prosopis velutina) and willow (Salix gooddingii). Some pools have seep-willow (Baccharis sarothroides) and spike rush (Carex spp.).

Figure 1. The study site ‘Agua Dulce’ Ramsar site (in red) located in the Sonoyta river.

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Usually the Sonoyta river flows once or twice a year during rainy season. It will have a strong current that usually lasts 3 or 4 days, then the flow decreases forming a narrow current that will keep water flowing for about a month (Figure 2); if rainy season is over the water level will keep decreasing forming pools that will endure for several months until most of them finally dry out, remaining just a few of them with enough water to keep aquatic species alive like the Sonoyta pupfish (Cyprinodon eremus), for the whole year until the next flow occurs. Also, there is a spring that provides water to the river during the whole year helping to keep a minimum level of water in some of the pools.

Figure 2. A narrow current flowing in the Agua Dulce Ramsar site part of the Sonyta river.

In the last 50 years the water level of the Sonoyta river has been decreasing dramatically due to groundwater depletion and loss of aquatic habitat (Rosen et al., 2010). Sonoyta is presumed to have had a cienega, and the Sonoyta River is thought to have originally had long-flowing reaches (Rosen et al., 2010). The reason for this decrease is mainly because of the overuse of ground water for agriculture in the Sonoyta Valley. Nowadays, the water level is so low in most part of the Agua Dulce Ramsar site that it only covers the body of an adult turtle partially which makes it easier to be detected by predators when they are active (Figure 3).

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Figure 3. Sonoyta Mud turtle in the Agua Dulce Ramsar Site. Water level is usually low enough to see part of the carapace out of the surface when a turtle is active.

METHODS

Mark-recapture technique During each sampling session, we walked through the river looking for Sonoran turtles, usually hidden in ponds along the river. Once captured, turtles were caught by hand. We used the method based on the one proposed by Cagle (1939), giving a serial number to each individual represented by marks in the marginal scutes. Thus, the scales on the right represent units from 1 to 9 and the scales on the left represent tens from 10 to 90, skipping the sixth and seventh scute (Figure 4). We used a dial caliper to measure the straight carapace length (SCL), curve carapace length (CCL), straight carapace width (SCW), and plastron width (PW) (Figures 5 and 6). We used a spring scale to obtain the weight of each individual (Figure 7). Gender (male or female) was determined by presence or absence of physical sexual characteristics; if sex was not clearly recognizable due to age, we recorded the individual as juvenile. We mapped the location of each individual turtle using a GPS unit and any unusual fact regarding behavior or physical characteristic present on the specimen. Finally, individual photos were taken of each turtle from above and underneath, to keep an image catalog of the captured individuals (Figure 8); also, pattern of the plastron may be used as a supplemental method of identifying individuals (Cross, et al. 2014).

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Figure 4. Marginal scutes marked. On the right side the second scale is marked representing a number 2 and on the left side the second scale is marked representing a 20, which means the turtle was assigned number 22.

Figure 5. Biologist Diego García measuring the length of a carapace in a Sonoyta Mud Turtle

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Figure 6. Recording data and taking measurements of capture turtles

Figure 7. Turtles were weighed using a spring scale

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Figure 8. Example of an individual photo of the individual #47 taken from underneath. Pattern of the plastron may be used as a supplemental method of identifying individuals.

Radiotelemetry monitoring In order to obtain information about the movements of the turtles in the study site we used the radiotelemetry technique (Hall and Steidl, 2007). Thus, we attached a VHF transmitter unit to the posterior costal scutes of 5 turtles using epoxy in order to follow their movements in the Agua Dulce site (Figure 4). We randomly chose each one of the individuals, recorded the location and measurements of each. We used radiotransmitters model PD-2 with a weight of 4gr, manufactured by Holohil Systems Ltd. (HSL). The battery of each transmitter had a lifespan of 3 to 4 months. Thus, during this time we visited the site looking for turtles with radio transmitter after the ‘mark-recapture’ search to avoid affecting detection probability during this effort. We located each individual using a radio receiver (Figure 5 and 6), and then we recorded the time and location using a GPS unit. Turtles were not handled after they were radio-marked.

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Figure 4. A VHF transmitter attached on one of the Sonoyta Mud Turtles

Figure 5. Use of radio receptor to look for the Sonoyta Mud Turtles

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Figure 6. Search of radio-marked turtles in the Agua Dulce site

Results Estimation of population size During the capture effort between 2016 and 2018 we captured a total number of 111 individual turtles within the Agua Dulce Ramsar Site, with 25 recaptures, in a total effort of 13 days; 1 day in 2016, 6 days in 2017 and 6 days in 2018. We captured the highest number of turtles in 2017 (n= 87), while in 2018 we captured just half of the number (n= 44) with the same sampling effort (Figure 7). We had 51 males, 55 females with a sex ratio of 1:1; 2 unidentified individuals, 3 juveniles and 5 yearlings (Figure 8). Also, during this time we found one individual dead for unknown reasons. Captures were done mainly from January to June (Figure 9). We had the highest number of captures in March (n= 34) in an effort of 5 days, while the lowest number was in June (n= 1) with only 1 day of effort. In November of 2017 we had the highest success with a 25 individuals captured in 1 day. Using the Schumacher-Eschmeyer method we estimated a population of 351 turtles with a variance of 0.3104, standard error of 0.000834, and with a 95% Confidence Interval the mean falls in an interval between 185.96 and 400. Also, using the Schnabel model we obtained an estimated population of 268 with a variance of 0.0557E-05 and a Standard

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Error of 0.000746. Records of the Sonoyta mud turtles appear widespread through the Agua Dulce site (Figure 10), but mainly close to the spring which is the beginning of the Ramsar site, upriver in the southeastern edge of the polygon.

100 90 80

70

60 50

40 No.of captures 30 20 10 0 2016 (1)* 2017 (6)* 2018 (6)* Year

Figure 7. Number of turtles captured by year. *Number of sampling days

Figure 8. Yearling turtle found in November of 2017.

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40

35

30

25

20

No.Captures 15

10

5

0 January February March April May June November 2* 2* 5* 1* 1* 1* 1* Month

Figure 9. Number of turtles captured by month between 2016 and 2018. *Number of sampling days

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Figure 10. Sonoyta Mud Turtles captured and marked during 2017 and 2018 at the

Agua Dulce Ramsar Site

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Movements and space use We quantified movements based on individuals that were radio-tagged in 2017 and 2018. Thus, we estimated the home range calculating the Minimum Convex Polygon (MCP) based on locations obtained in the field (Mohr, 1947) and the length of the path using the extension Hawth’s Tools for ArcGIS 9.3. For year 2017 all five tagged individuals were used to obtain a MCP, but for individuals tagged in 2018 only two had enough records to create a MCP. For both years tagged individuals had a mean size of their MCP of 0.0856 ha and paths with a mean length of 172.99 m. Females had a mean home range of 0.122 ha and males 0.0379 ha; with a mean length of path of 238.7m and 90.84m respectively.

Table 2. Size of the Minimum Convex Polygon calculated and Length of path of each individual in 2017

Size of the Minimum Length of path Transmitter Gender VHF Frequency Convex Polygon (ha) (m) T1 Female 150.990 0.1824 473.47 T2 Male 150.301 0.0819 196.76 T3 Female 150.500 .066 347.01 T4 Female 150.700 .1341 225.22 T5 Female 150.900 .1042 146.51

Table 3. Size of the Minimum Convex Polygon calculated and Length of path of each individual in 2018

Size of the Minimum Length of path Transmitter Gender VHF Frequency Convex Polygon (ha) (m) T6 Male 152.080 - - T7 Male 152.120 0.0111 64.83 T8 Male 152.178 - 30.08 T9 Male 152.301 0.0206 71.71 T10 Female 152.040 - 1.3

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Figure 11. Movements of radio-marked Sonoyta Mud Turtles in 2017 at the Agua Dulce Ramsar Site (T: Transmitter, MCP: Minimum Convex Polygon, Loc: Location).

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Figure 12. Movements of radio-marked Sonoyta Mud Turtles in 2018 at the Agua Dulce Ramsar Site (T: Transmitter, MCP: Minimum Convex Polygon, Loc: Location).

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DISCUSSION The Sonoyta river water flow has been decreasing in the last decades, and habitat quality for the Sonoyta mud turtle is deteriorating. Having a population of 350 individuals in the Agua Dulce Ramsar site is relevant for conservation purposes and to keep a genetic variation. This monitoring effort should be kept in Agua Dulce for long term in order to know how this population is behaving and have a better idea on how the variation of water level is affecting the survival and reproduction of Sonoyta mud turtles. Although, for future mark and release studies within this site, it will be necessary to use the same marks in order to avoid double-marking individuals. During summer of 2017 we had a strong flow in the Sonoyta River. We compared movements of turtles before and after the flow and the five radio-tagged individuals remained in the same spot. The Agua Dulce RAMSAR site is connected through the Sonoyta River to the waste water treatment plant located 17 km upriver near to the town of Sonoyta, and also connected to the Quitobaquito spring, which is about 1.5km away but separated by a highway. Information obtained with radiotelemetry provides no evidence of turtles leaving their pool after a strong flow occurred, so we did the estimation of the population size of Agua Dulce assuming that there is not migration from outside of this site. We did not find evidence of females nesting but we know reproduction is happening after catching 5 yearlings during fall of 2017. Also, in March 30th we found turtles actively moving and searching for a mate. We believe there is a good number of Sonoyta Mud Turtles in the Agua Dulce Ramsar site, more than we expected, but it will be necessary to have a plan to improve the habitat in order to maintain this and other populations of aquatic species.

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Literature cited Cross, D. M., G. J. Lipps, J. M. Sapak, E. J. Tobin, K. V. Root. 2014. Pattern-Recognition Software as a supplemental Method of Identifying Individual Eastern Box Turtles (Terrapene c. Carolina). Herpetological Review. 45 (4). 584-586. Society for the Study of Amphibians and .

Hall, D. H., Hall and R. J. Steidl. Movements, Activity, and Spacing of Sonoran Mud Turtles (Kinosternon sonoriense) in Interrupted Mountain Streams. Copeia, 2007 (2), pp- 403-412.

Iverson, J.B. 1981. Biosystematics of the Kinosternon hirtipes species group (Testudines: Kinosternidae). Tulane Studies in Zoology and Botany 23:1-74.

Peterson and Stone, 2000. Physiological capacity for estivation of the Sonoran mud turtle, Kinosternon sonoriense. Copeia 2000:684-700.

Lignon, D. B., and C. C. Peterson. 2002. Physiological behavioral variation in estivation among mud turtles (Kinosternon spp.). Physiological and Biochemical Zoology 75:283-293.

Mohr, C.O. 1947. Table of equivalent populations of North American small mammals. American Midland Naturalist 37: 223-249.

National Park Service. 2016. 2016 Status of the Sonoyta Mud Turtle. Organ Pipe Cactus National Monument. National Park Service. U.S. Department of the Interior.

Ramsar. 2008. Ficha Informativa de los Humedales de Ramsar (FIR)- Versión 2006-2008 http://www.ramsar.org/ris/key_ris_index.htm

Ramsar. 2018. The List of Wetlands of International Importance. Published 13 June 2018. 54pp. https://www.ramsar.org/sites/default/files/documents/library/sitelist.pdf

Rosen, P. C., Melendez, C., Riedle, J. D., Pate, A. C., and Fernandez, E. 2010. Ecology and conservation in the Sonoyta Valley, Arizona and Sonora. In: W. Halvorson, C. Schwalbe, and C. van Riper III (eds), Southwestern Desert Resources, pp. 143-160. University of Arizona Press, Tucson.

SEMARNAT. 2010. Norma Oficial Mexicana NOM–059–ECOL–2010, Protección ambiental– Especies nativas de México de flora y fauna silvestres– Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio– Lista de especies en riesgo. Diario Oficial de la Federación, segunda sección, jueves 30 de diciembre de 2010.

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Stone, P. A. 2001. Movements and demography of the Sonoran Mud Turtle, Kinosternon sonoriense. Southwestern Naturalist 46:41-53.

U.S. Fish and Wildlife Service 2016. Species Status Assessment Report for the Sonoyta Mud turtle Version 1.0. August 2016. USFWS, Region 2. Albuquerque, NM

Van Dijk, P.P. 2011. Kinosternon sonoriense. The IUCN Red List of Threatened Species 2011: e.T11011A97382186. http://dx.doi.org/10.2305/IUCN.UK.2011- 1.RLTS.T11011A3238623.en

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