BIOLOGICAL CONSERVATION 130 (2006) 386– 393

available at www.sciencedirect.com

journal homepage: www.elsevier.com/locate/biocon

No place to nest or bask: Effects of human disturbance on the nesting and basking habits of yellow-blotched map ( flavimaculata)

Megan J.C. Moore1, Richard A. Seigel*

Department of Biological Sciences, Southeastern University, Hammond, LA 70403-0736, USA

ARTICLE INFO ABSTRACT

Article history: Considerable recent attention has focused on how human disturbance alters the behav- Received 20 July 2005 iour of imperiled taxa. Data on such impacts are common for waterfowl, marine mam- Received in revised form mals, and some large game . However, little is known about how human 20 December 2005 disturbances affect , perhaps because most reptiles are secretive and are not Accepted 4 January 2006 commonly seen by the public. We studied the impact of human disturbances on the Available online 6 March 2006 nesting and basking behaviour of the yellow-blotched map (Graptemys flavimaculata) on the Pascagoula River in southeastern , USA. We found that both nesting Keywords: and basking behaviour of map turtles were altered by human recreational activities. Tur- Nesting tles attempting to nest commonly abandoned their attempts upon the approach of a boat Basking and, prior to nesting, numerous individuals waited several hours near the beach without Human disturbances emerging. Basking turtles frequently dove into the water upon the approach of a boat Map turtles and some did not return to bask. Anglers in small boats that remained in the vicinity of basking sites caused the most disturbances, whereas personal water crafts (jet skis) caused fewer disturbances. Our data suggest that interruption of nesting activities may have an especially severe impact on the viability of this population through changes in numbers of clutches females are able to lay and altering the microhabitat females select for their nests. 2006 Elsevier Ltd. All rights reserved.

1. Introduction Schwikert, 2002), marine mammals (Constantine et al., 2004; King and Heinen, 2004), and large terrestrial game species Although habitat destruction or modification and the intro- (Stockwell et al., 1991) indicated that human disturbance duction of invasive species are generally considered to be can significantly alter feeding schedules, habitat use, and among the most important threats to biodiversity (Foin time spent nursing young. Even though the population conse- et al., 1998), considerable attention recently has focused on quences of such disturbances often are not known, changes the ways in which human disturbance alters the behaviour in behaviour and habitat use concern conservation biologists of imperiled taxa (see review in Frid and Dill, 2002) and and wildlife managers. whether such alteration leads to reduced population sizes Despite the wealth of information available for birds and (Gill et al., 1996; Beale and Monaghan, 2004). Studies on organ- mammals, comparatively little is known about how human isms as diverse as waterfowl (Gill et al., 1996; Rodgers and disturbances affect reptiles, perhaps because most reptiles

* Corresponding author: Present address: Department of Biological Sciences, Towson University, 8000 York Road, Towson, MD 21252, USA. Tel.: +1 410 704 3123; fax: +1 410 704 2405. E-mail address: [email protected] (R.A. Seigel). 0006-3207/$ - see front matter 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2006.01.001 BIOLOGICAL CONSERVATION 130 (2006) 386– 393 387

are secretive and are not commonly seen by the public (but see Johnson et al., 1996; Hecnar and M.’Closkey, 1988; Parent and Weatherhead, 2000). However, in many aquatic habitats, freshwater turtles are frequently seen basking and nesting, especially in river systems where human recreational activi- ties are common. Direct harassment of basking turtles by rec- reational shooters (‘‘plinking turtles’’) is a well-known activity in much of North America (Ernst et al., 1994) and has obvious negative impacts. The ways by which less overt disturbances affect aquatic turtles is poorly known, but given the rapid de- cline seen in many turtle species throughout the world (Gib- bons et al., 2000), data on such impacts clearly are needed. From 1993 to 1997, we studied the behavioural and repro- ductive ecology of the yellow-blotched map turtle (Graptemys flavimaculata) on the Pascagoula River in southeastern Missis- sippi, USA. This turtle underwent a severe decline in the 1980s and is currently listed as Threatened under the US Endangered Species Act of 1973, as amended. One of the ma- jor factors contributing to this decline is human disturbance, especially on sandbars where this species nests (U.S. Fish and Wildlife Service, 1991). Here, we report information on nest- ing and basking behaviour in this species, specifically on the impacts resulting from human disturbance. Further, we make recommendations to area managers as to how these impacts could be minimized.

2. Methods Fig. 1 – Study site on the Pascagoula River located within the Our research was conducted within the Ward Bayou Wildlife Ward Bayou Wildlife management area in Jackson Co., MS. Management Area in a small portion of the Pascagoula River near Vancleave, Jackson County, Mississippi (Fig. 1). Two boat landings, located 5.0 km upstream and 10.6 km downstream tions were conducted during each hour. Because of the of the study site, function as a source for human activity. difficulty in maintaining positive identification of unmarked We studied a 300 m section of the river, which included both submerged turtles, it was often not possible to determine if a nesting beach (Beach #7) on the west bank and a basking a female was making her first nesting attempt, or had previ- area along the east bank (Fig. 1). The nesting beach was a ously attempted nesting but abandoned her effort(s). As a re- sandbar approximately 50 m long by 10 m wide and about sult, if positive identification could not be made, it was 1 m high, with low herbaceous vegetation. Across the river assumed that the observation was of a new individual making from the nesting beach was a steep cut bank with numerous her first attempt. Therefore, the number of reported females fallen trees and branches used as basking substrates by G. attempting to nest is likely too high, but the number of nest- flavimaculata. Most basking structures were separated by 1 ing attempts observed is accurate. Nesting activities were or 2 m from the shore. A detailed description of river dimen- separated into six categories: pre-nest activity, locate nest sions, annual mean discharge rates, and substrate composi- site, excavate nest, lay eggs, bury nest, and return to water. tion can be found in Brauman (1995) and Jones (1996). Times for each activity were recorded to the nearest whole minute. During the 1998 field season, all observed distur- 2.1. Effects of human disturbance on nesting bances from humans and the reaction of the turtles to those disturbances were documented. Date, time, type of water- Disturbance of nesting was determined via observation from craft, and purpose in the area (e.g. fishing, playing, passing a blind (1.2 m · 1.2 m · 1.7 m) set up in one of two locations, through, picnic or camping) were recorded. either directly across the river from Beach #7 or on the south end of Beach #7 (Fig. 1). We conducted observations for a min- 2.2. Effects of human disturbance on basking imum of 4 h at a time at irregular intervals between 05:00 and 19:00 h using a 60 · 114 spotting scope with tripod, and we did We conducted observations from 28 May 1997 to 13 July 1998, not conclude until at least one hour past the last nesting with a minimum of one day of observation per week, except event. Hourly air temperature and daily water temperature for January and February 1998 when high water precluded measurements were recorded to the nearest 0.1 C using a such observations. A blind (1.2 m · 1.2 m · 1.7 m) was set up Miller and Weber quick reading thermometer. immediately before observations began, and was placed The numbers of nest attempts were standardized per hour across the river from the basking logs at the edge of the of observation (unit of effort) by dividing the number of ob- woods (Fig. 1). Because of the proximity of the basking site served attempts per hour by the number of times observa- to the nesting sandbar, disturbances to basking were the 388 BIOLOGICAL CONSERVATION 130 (2006) 386– 393

same as those experienced by nesting turtles. As a result, over six and a half hours (404 min; mean = 159.9 ± 95.6 min) observations of basking and disturbance were conducted sim- before attempting to nest. One female waited at least ilarly to observations of nesting and disturbance, except that 622 min without nesting before observations were terminated. observations did not extend past 17:00 h. We recorded the During 54 days of nesting observations, pre-nesting females numbers of turtles basking in 15-min intervals or immedi- never emerged onto the beach during 36 of these days ately before and after a disturbance, whichever came first. Be- (66.6%) (mean = 3.1 ± 2.5 turtles/day, range 0–13), The total cause females were much larger than males and have a time for pre-nesting might be much longer than indicated distinct shell morphology, we recorded the number and sex above, as turtles could have been waiting several days to nest of each individual on each basking log. before we began observations. Timing of each nesting foray began when each female was fully exposed on the nest beach 2.3. Data processing and statistical analysis and concluded when each female re-entered the river. Total exposure time among females that entered the beach and Data were entered into Microsoft Excel and statistical analy- completed oviposition averaged 34.6 ± 11.5 min (range = 22– ses were carried out on SYSTAT v10.0 and S-Plus 4.5. We used 60). At this location, yellow-blotched map turtles needed a chi-square contingency table analysis, Student’s t-test, two- mean time of 3.7 ± 3.7 min (range = <1–13) to locate a nest site. way ANOVA, and a Mann–Whitney U-test for analysis among The mean time to excavate a nest, deposit the eggs, and bury season, sex, or disturbance types. To ensure independence of the nest was 11.2 ± 1.6 min (range = 9–14), 5.2 ± 2.0 min the data, we used only the first observation of the day when (range = 3–9), and 14.1 ± 8.0 min (range = 6–29) respectively. reporting disturbance to basking turtles. To meet standards The amount of time to return to the water was less than a min- of normality a square root transformation was performed ute for all nesting observations. Timing of nesting observa- on the number of basking turtles prior to running the two- tions at other locations were not recorded, so these times way ANOVA. Means are followed by ±SD; a was set at 0.05 could vary by location. for all statistical tests. 3.2. Effects of human disturbance on nesting 3. Results Numerous yellow-blotched map turtles attempted to nest on 3.1. Nesting behaviour and timing of nesting Beach #7 but, as a result of various forms of disturbance, they frequently abandoned their efforts and retreated to the water. We logged >270 h of observations of turtle nesting behaviour We observed a total of 79 nesting attempts, of which only 15 during 1997 and 1998. All nesting attempts occurred between (19%) successfully completed oviposition. Known numbers of 06:11 and 16:49 h, with a peak number of occurrences (48%) be- nesting attempts of a single individual prior to completion tween 15:00 and 17:00 h (Fig. 2). Of 15 females seen to nest suc- ranged from one to six. cessfully, we had an unobstructed view of 10 (eight from 1997 More than 95 h of observation were logged from 20 May to and two from 1998), and we documented the details and dura- 14 July 1998 to record human disturbance of nesting females. tion of each nesting event. Females waited in the water A total of 130 disturbances were recorded, which included ‘‘watching’’ the beach prior to nesting for lengthy periods of several events when an angler in a small boat would remain

1.2

1.0

0.8

0.6

Nests per hour 0.4

0.2

0.0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 05 06 07 08 09 10 11 12 13 14 15 16 17 18 Time of day

Fig. 2 – Number of nesting attempts by Graptemys flavimaculata per standardized hour of observation. BIOLOGICAL CONSERVATION 130 (2006) 386– 393 389

near the nesting beach for an extended period of time (to of basking than the other seasons. However, a strongly signif- 50 min). Disturbances were so frequent on or near the nesting icant interaction between gender and season (F = 6.04, df = 3, beach that the median time between disturbances was actu- 70, P = 0.001) means that two sexes responded differently to ally 0 min (Fig. 3). Disturbances per day varied and ranged seasonal effects. The basking rates for males were highest from a high of more than one disturbance every minute to a in the fall, whereas basking rates for females were highest low of one disturbance every 338 min (5.6 h). Of the 17 days in the spring. of observation, only eight days (47.0% of weekdays) had en- G. flavimaculata began basking as early as 06:00 h and con- ough time (34.6 min) between disturbances for females to tinued throughout the day until at least 18:00 h (when routine complete oviposition once they were actually on shore. How- observations ceased) and occasionally until nightfall (B. ever, our weekday data likely considerably underestimate the Horne, pers. comm.). Daily basking patterns of both males effects of human disturbance because boat traffic was so and females during the spring revealed a unimodal relation- much greater on weekends that it prevented sampling. In ship, peaking near 12:30 h (Moore, 2003). During the summer, the absence of human activities, females were disturbed dur- daily basking patterns of female yellow-blotched map turtles ing nesting 12.1% of the time by fish crows (Corvus ossifragus; appear to be bimodal, with peaks during both mid morning N = 58 unsuccessful attempts) and spontaneously abandoned and mid afternoon respectively. Concurrently, males have a their nesting attempts (N = 58 unsuccessful attempts) 8.6% of unimodal basking pattern with a peak around 12:00 h when the time. female basking declines temporarily (Moore, 2003). Basking In addition to disturbing and or delaying the nesting pro- during the fall was somewhat reduced compared to spring cess of yellow-blotched map turtles, humans also directly im- and summer and had a unimodal peak at 12:45 h (Moore, pacted nests by trampling on one nest, creating a campfire 2003). above another nest, dumping ice onto nests, and destroying five more nests by digging up the covers designed to prevent 3.4. Effects of human activity on basking predation. We recorded more than 118 h of observations during 23 days 3.3. Timing and intensity of basking from 1 March to 14 July 1998 to observe human disturbance of basking turtles. Six weekend (Friday, Saturday, and Sunday) We logged more than 159 h of observations on basking behav- observations occurred from 1 March to 2 May, prior to the iour during 39 sampling days from 19 June 1997 to 13 July nesting season, whereas 17 weekday (Monday–Thursday) 1998. Yellow-blotched map turtles basked throughout the observations occurred during the nesting season (20 May to year, but the number of turtles basking varied considerably 13 July). Recovery times (time to return to basking sites among months/seasons. The mean number of basking map post-disturbance) were recorded from 2 May to 13 July 1998. turtles was lowest in December (0.03 turtles/count), but was On a typical weekday, we observed 2–8 passing boats per considerably higher from April through November, with a hour, ranging from flat bottom boats, to personal water craft peak in April (15.8 turtles/count; see Moore, 2003 for details). (PWC [jet-skis]), to speedboats. On weekends and holidays, A two-way ANOVA showed that there were no significant ef- boat traffic became much heavier. The mean number of boat fects of sex on basking rates (F = 0.266, df = 1, 70, P = 0.608), disturbances peaked at the same time of day when female but basking rates differed strongly among seasons (F = 5.45, basking decreased (Fig. 4). A total of 210 disturbances were re- df = 3, 70, P = 0.002), with winter having a much lower rate corded during all observation periods, which included several

225

200

175

150

125

100

75

50 frequency of disturbances frequency 25

0

-5 0 5 0 5 0 5 0 5 0 0 0 0 0 0 -1 -1 -2 -2 -3 -3 -4 -4 -5 0 0 0 0 6 1 6 1 6 1 6 1 6 -1 -2 -3 -4 1 1 2 2 3 3 4 4 0 1 1 1 5 0 0 0 1 2 3 minutes between disturbances

Fig. 3 – Median amount of time elapsing between disturbances while nesting. 390 BIOLOGICAL CONSERVATION 130 (2006) 386– 393

events when an angler remained in the area for an extended individuals because of similar numbers of each gender and period of time (up to 50 min). The median amount of time be- relative sizes both before and after each disturbance. The tween disturbances was only 3 min. overall recovery rate (number of turtles returning to the logs It was rare to observe basking without some form of dis- /number of turtles disturbed) was 77.0%. The mean recovery turbance. However, during undisturbed periods, a few turtles time was 20.5 ± 26.7 min (n = 221, range = 2–189 min). would spontaneously abandon basking, but typically the Although not significant, the mean recovery time of females number of female turtles we observed between count inter- was nearly two-thirds as long as males (mean male recov- vals increased (mean increase = 1.17 ± 3.25 turtles/period). ery = 28.189 min, mean female = 18.924 min; t = À1.937, df = Conversely, passage of a boat caused at least one basking tur- 218, P = 0.053). tle to dive into the water on 65 of 119 occasions (54.6%). On an additional 20 occasions (16.8%), disturbances prohibited tur- 4. Discussion tles from re-emerging onto basking sites while humans re- mained within the immediate vicinity. The percent of 4.1. Effects of human disturbance on nesting behaviour turtles abandoning basking sites varied from 0% to 100% (mean = 69.0 ± 33.3%, N = 119 observations) per disturbance. As is true of waterfowl and some marine mammals, we found Females were more likely to abandon their basking site than that the behaviours of yellow blotched map turtles were al- males (X2 = 18.781, df = 1, P < 0.001). Additionally, the number tered by human recreational activities. Turtles attempting to of turtles disturbed differed significantly with the type of dis- nest commonly abandoned their attempts upon the approach turbance (X2 = 22.82, df = 2, P < 0.001; Table 1). Specifically, an- of a boat. Prior to nesting, numerous individuals waited sev- glers that remained in the basking vicinity caused the most eral hours near the sandbar without emerging to nest. Be- disturbances (74%), but PWCs caused less than an expected cause of perceived threats or disturbances, females had less amount of disturbance (37%). In fact, although many turtles than a 19% chance of successfully completing oviposition fell into the water when PWCs briefly passed through the once they emerged onto the beach. On some days, distur- area, a few continued to bask even when the PWCs stayed bances by boat traffic were nearly continuous. Even on the within the basking vicinity for extended periods. most conservative basis (i.e., counting only weekdays and On many occasions turtles that abandoned basking after only using the time it takes a female to nest between emer- being disturbed by boats returned to basking logs after a gence onto the sandbar and return to the water), we found recovery period. Although we cannot rule out that new indi- that only 53% of days during the nesting season had sufficient viduals may be exploiting newly available basking sites after time between disturbances to accommodate nesting. Because a disturbance, it was presumed that these were the same disturbances were more frequent on weekends (pers. obs.) and because females spent considerable time observing bea- ches before nesting, the number of days available with en- 9 7 ough undisturbed time to complete nesting was much lower

8 Disturbance 6 than 53%. female M

7 e

a Another indicator that boating activities were influencing n male 5 d

6 i n s t u nesting behaviour in map turtles was the relatively short u m 5 4 r b b a

e amount of time it took this species to nest. By comparison n 4 r 3 c o e f s with other emydid turtles, G. flavimaculata nest quickly (Table

3 b 2 o a

2 t 2). Shortened nesting times may be explained by one of two 1 Mean number of turtles 1 possible explanations. (1) The location of the nest site could 0 0 have been determined on a previous nest attempt, thus 0 0 0 0 0 0 0 0 0 0 0 0 0 0 :0 :0 :0 :0 :0 :0 :0 :0 :0 :0 :0 :0 :0 :0 5 6 7 8 9 10 11 12 13 14 15 16 17 18 speeding the total nesting time. Among the 15 turtles to suc- Time cessfully nest, at least six of the females had a minimum of one previously failed nest attempt, and retreated due to some Graptemys Fig. 4 – Mean number of basking female and male form of human disturbance or other perceived predator. (2) flavimaculata per hour plotted with mean number of boat The speed to locate and complete oviposition has been se- disturbances per hour of the day from 1 March to 13 July lected as a mechanism with which to avoid various distur- 1998. bances. The first explanation only accounts for the time needed to locate a nest site and infers that the females retain a memory of nest site location. Christens and Bider (1987) re- ported some Chrysemys picta explored suitable nesting habitat Table 1 – Relationship between type of disturbance and the percent of basking Graptemys flavimaculata disturbed and returned to the water before actually nesting in the sub- sequent hours or days post-exploration. However, even if nest Disturbance type % Disturbed % Undisturbed N site selection times were equivalent among species of emyd- Anglers (setting trot lines) 74 26 61 ids, G. flavimaculata would still be considerably faster (Table 2). Sound of gunshots 73 27 15 The second explanation infers that individuals in this popula- Passing speed boat 67 33 9 tion have adjusted their behaviour to minimize exposure to Personal water craft (PWC) 37 63 202 potential disturbances. Moll (1974) noted an interesting obser- Passing jonboat 28 72 741 vation of an undisturbed population of basking painted tur- Stopping at beach 19 81 11 tles that appeared less wary of humans than disturbed BIOLOGICAL CONSERVATION 130 (2006) 386– 393 391

Table 2 – Summary of nesting times of turtle species in the family Species Time of day Search for site Dig Lay Bury Total Source

Clemmys guttata Late afternoon–early evening 29–75 12.5–22.4 – 45–120 Ernst (1970) Chrysemys picta Late afternoon–early evening – – – – 90 Christens and Bider (1987) Emydoidea blandingii Night 13 16 13 95 150 Linck et al. (1989) muhlenbergii Late afternoon–early evening 29 26 9 50 165 Holub and Bloomer (1977) Glyptemys insculpta Late afternoon–early evening 94+ 9 46 180–240 Pallas (1960) Graptemys flavimaculata Daytime (mid-afternoon) 3.7 11.2 5.2 14.1 34.6 Moore, pers. obs. Graptemys nigrinoda Nighttime min–h 23 8–10 20 60–180 Lahanas (1982) Malaclemys terrapin Daytime 7? 8 2 9 26? Burger (1977) Terrapene carolina Mostly evening 300 Congello (1978) scripta Early morning or late evening 26–187 Cagle (1950)

Times listed for Graptemys flavimaculata are means from 10 nesting turtle observations. All times are listed in minutes. populations. This observation suggests an ability of the tur- 4.3. Impacts on population viability tles to modify their behaviour to avoid disturbances while nesting. Given the frequency of disturbances on the Pasca- Although the impacts of boating activities on birds and mam- goula River, a faster nesting speed could minimize exposure mals have been well-documented (e.g., Stockwell et al., 1991; to potential threats, and may be a partial explanation of their Gill et al., 1996; Rodgers and Schwikert, 2002; Beale and Mona- rapid nesting speed. ghan, 2004; Constantine et al., 2004; King and Heinen, 2004), our study is apparently the first detailed account of human 4.2. Effects of human disturbance on basking recreational activities on freshwater turtles. The closest par- allel to our data appears to be for loggerhead sea turtles (Car- The impact of boating activities on basking behaviour is per- etta caretta), where organized ‘‘turtle watches’’ slightly altered haps increased by the gregarious nature of turtles basking to- nesting behaviour, but did not result in changes in egg pro- gether on limited space, which provides an increased duction or success (Johnson et al., 1996). Similarly, Parent awareness of predators. A solitary basking turtle may not be and Weatherhead (2000) found few negative effects of human aware of nearby potential threats (Auth, 1975). However when disturbance on massasauga rattlesnakes (Sistrurus catenatus), basking in groups, the stimulus of an individual dropping into although some movement patterns were altered. the water often causes the others to abandon their basking As is true of many of studies cited above, our data suggest, activity (Shealy, 1976). In our study, basking turtles frequently but cannot conclusively prove, that the demonstrated retreated into the water and many did not return to their changes in nesting and basking activity are having a negative basking sites following disturbance by boats or PWC. In fact, impact on yellow-blotched map turtles. Our study population disturbances happened so frequently (an average of one every is notable for two unusual reproductive conditions, a high fre- 3 min during peak periods), that at least 13% of turtles dis- quency of nests constructed in low-quality habitats and a low turbed by boats never returned to bask, and, of those that frequency of multiple clutches (Horne et al., 2003). Both con- did return, an average of 20 min was needed to re-initiate ditions could be the direct or indirect result of high levels of basking, which was more time than was often available be- human disturbance. For example, many females in this pop- fore the next disturbance. Although perhaps coincidental, ulation lay their eggs on heavily shaded and steep sided clay our data show that the numbers of female turtles basking de- banks, where low soil temperatures preclude the production creases at the same time of day when boating activity peaks of female hatchlings (Horne et al., 2003). We have witnessed (Fig. 4). However, whether females reduced their basking ef- females in such conditions in which they have fallen back forts because of boat disturbances or some other factor can- repeatedly into the river while attempting to nest on steep not be determined. slopes (P45). We suggest that the use of such low quality Anglers in small boats that remained in the vicinity of nesting sites is at least partially due to the high levels of dis- basking sites caused the most disturbances, whereas PWCs turbance on more appropriate nesting beaches (Horne et al., caused fewer disturbances (Table 1). This result is likely due 2003). Because nesting events are energetically costly (Shine, to the close distance of anglers to the basking logs and the 1980; Schwarzkopf and Shine, 1991; Swimmer, 1997), females long period they remained near the basking site, both of that are forced to increase the number of nesting attempts which would cause turtles to bask less. Conversely, distur- due to disturbances will have to invest more time and energy bances from PWCs could be placed into one of two categories: than do females that are not disturbed. Therefore, human dis- (1) brief disturbances as they quickly passed through the area, turbance likely increases the energetic cost of nesting. or (2) riders remaining in the area for wave jumping, joy rid- Secondly, the low frequency of multiple clutches could ing, and playing on the beach. Likewise, many turtles reacted partially stem from the loss of basking time and subsequent to the two forms of PWC disturbance differently. They either lowered body temperatures. Increased body temperatures by all immediately retreated into the water when PWCs briefly basking increases digestion rates, speeds development of ovi- passed through the area, or many turtles dropped into the ductal eggs, and helps eliminate external parasites (Gatten, water, while a few continued to bask and appeared somewhat 1974; Vogt, 1979; Parmenter, 1981; Whittow and Balazs, 1982; habituated to the PWCs activity. Hammond et al., 1988; Avery et al., 1993; Swimmer, 1997). 392 BIOLOGICAL CONSERVATION 130 (2006) 386– 393

Although we lack data on turtle body temperatures at our site, for this work were granted by the US Fish & Wildlife Service it is likely that individual body temperatures decreased as tur- and the Mississippi Department of Wildlife, Fisheries, and tles dropped from basking logs into the river. Water tempera- Parks. This work was performed under the approval of the tures in the Pascagoula River in May and June ranged from 22 Care Committee of Southeastern Louisiana University. to 27 C (pers. obs.), whereas individuals basking at this time of year might have body temperatures in excess of 32 C(Spo- tila et al., 1990). Interruption of basking and consequent REFERENCES reduction in body temperature has the potential to impact the ability of individual turtles to process and digest food, and the ability of females to develop eggs during the repro- Auth, D.L., 1975. Behavioral ecology of basking in the ductive season. yellow-bellied turtle, Chrysemys scripta (Schoepff). Bulletin of the State Museum. Biological Sciences 20, 1–45. 4.4. Management implications Avery, H.W., Spotila, J.R., Congdon, J.D., Fischer Jr., R.U., Standora, E.A., Avery, S.B., 1993. Roles of diet protein and temperature in Yellow-blotched map turtle populations have undergone a se- the growth and nutritional energetics of juvenile slider turtles, vere decline, although the causes of decline are poorly known Trachemys scripta. Physiological Zoology 66, 902–925. (Horne et al., 2003). Our data provide examples of how hu- Beale, C.M., Monaghan, P., 2004. Behavioural responses to human disturbance: a matter of choice. Animal Behaviour 68, mans detrimentally affect this population, especially in the 1065–1069. form of disturbance from boat traffic while turtles are nesting Brauman, R.J., 1995. The female reproductive biology, nesting and basking. As a result, the following recommendations are habits, and conservation biology of the yellow-blotched map provided for the conservation and management of this turtle, Graptemys flavimaculata. Unpubl. M.S. Thesis, population. Southeastern Louisiana University, Hammond, LA. Female G. flavimaculata need lengthy uninterrupted periods Burger, J., 1977. Determinants of hatching success in to bask and nest successfully. Management should be directed , Malaclemys terrapin. American Midland Naturalist 97, 444–464. toward reducing human disturbances on the 11 km stretch of Cagle, F.R., 1950. The life history of the slider turtle, the Pascagoula River where nesting is most common (Horne scripta trootsii (Holbrook). Ecological Monographs 20, 31–54. et al., 2003). Specifically, anglers, recreational boaters, and Christens, E., Bider, J.R., 1987. Nesting activity and hatching PWCs should be banned or have only limited access to the success of the (Chrysemys picta marginata)in areas immediately adjacent to the nesting beaches. This rec- southwestern Quebec. Herpetologica 43, 55–65. ommendation will be controversial, as recreational boating Congello, K., 1978. Nesting and egg laying behavior in Terrapene carolina. In: Proceedings of the Pennsylvania Academy of is extremely popular in southern Mississippi. Because anglers Sciences, vol. 52, pp. 51–56. cause the most disturbances to basking yellow-blotched map Constantine, R., Brunton, D.H., Dennis, T., 2004. Dolphin-watching turtles and are required to comply with natural resource man- tour boats change bottlenose dolphin (Tursiops truncates) agement regulations, they may be the easiest group to regu- behaviour. Biological Conservation 117, 299–307. late. We suggest limiting permits to fit the above timeline Ernst, C.H., 1970. Reproduction in Clemmys guttata. Herpetologica and location restrictions. We also suggest that recreational 26, 228–232. river use by all boat types could be restricted to four days a Ernst, C.H., Lovich, J., Barbour, R.W., 1994. Turtles of the United States and Canada, second ed. Smithsonian Institution Press, week, giving the turtles at least three undisturbed days to bask Washington, DC. and or nest. This option presents a compromise that should Foin, T.C.,Riley, S.D., Pawley, A.L., Ayres, D.R., Carlsen, T.M.,Hodum, provide a concentrated block of time for this species’ needs. P.J., Switzer, P.V., 1998. Improving recovery planning for Although activity such as camping and picnicking has been threatened and endangered species. BioScience 48, 177–184. restricted on some of the nesting beaches (R. Jones, pers. Frid, A., Dill, L., 2002. Human-caused disturbance stimuli as a comm.), enforcement of such regulations is critical in prevent- form of predation risk. Conservation Ecology 6, 11 http:// ing alteration of nesting habits (Jones, in press). www.ecologyandsociety.org . Gatten Jr., R.E., 1974. Effect of nutritional status on the preferred body temperature of the turtles Pseudemys scripta and Terrapene Acknowledgements ornata. Copeia 1974, 912–916. Gibbons, J.W., Scott, D.E.., Ryan, T.J., Buhlmann, K.A., Tuberville, We are most grateful to R. Jones for inviting us to participate in T.D., Metts, B.S., Greene, J.L., Mills, T., Leiden, Y., Poppy, S., this project and for lending us his expertise on map turtles, Winne, C.T., 2000. The global decline of reptiles, deja vu amphibians. BioScience 50, 653–656. Funding was provided by the US Army Corps of Engineers, Gill, J.A., Sutherland, W.J., Watkinson, A.R., 1996. A method to the US Fish & Wildlife Service, and the Mississippi Department quantify the effects of human disturbance on animal of Wildlife, Fisheries, and Parks, and we thank R. Jones, L. LaC- populations. Journal of Applied Ecology 33, 786–792. laire, and B. Peck for their support. Additional funding and Hammond, K.A., Spotila, J.R., Standora, E.A., 1988. Basking behavior support was provided by the Department of Biological Sci- of the turtle Pseudemys scripta: effects of digestive state, ences of Southeastern Louisiana University, especially G. Chil- acclimation temperature, sex. Physiological Zoology 61, 69–77. ders and N. Norton. We thank the many students who assisted Hecnar, S.J., Mcloskey, R.T., 1988. Effects of human disturbance on five-lined skink, Eumeces fasciatus, abundance and with this project, especially R. Brauman, B. Horne, R. Fiorillio, distribution. Biological Conservation 85, 213–222. J.S. Doody, T. Escalona, and C. Strong. Additionally we thank R. Holub, R.J., Bloomer, T.J., 1977. The , Clemmys Moore for generating the map of the study site. R. Jones, B. muhlenbergii...a natural history. Bulletin of the New York Horne, and two reviewers helped improve the ms. Permits Herpetological Society 13, 9–23. BIOLOGICAL CONSERVATION 130 (2006) 386– 393 393

Horne, B.D., Brauman, R.J., Moore, M.J.C., Seigel, R.A., 2003. Rodgers Jr., J.A., Schwikert, S.T., 2002. Buffer-zone distance to Reproduction and nesting ecology the yellow-blotched map protect foraging and loafing waterbirds from disturbance turtle, Graptemys flavimaculata: implications for conservation by personal watercraft and outboard-powered boats. and management. Copeia 2003, 729–738. Conservation Biology 16, 216–224. Johnson, S.A., Bjorndal, K.A., Bolten, A.B., 1996. Effects of Schwarzkopf, L., Shine, R., 1991. Thermal biology of reproduction organized turtle watches on loggerhead (Caretta caretta) in viviparous skinks, Eulamprus tympanum: why do gravid nesting behavior and hatchling production in Florida. females bask more. Oecologia 88, 562–569. Conservation Biology 10, 570–577. Shealy, R.M., 1976. The natural history of the map turtle, Jones, R.L., 1996. Home range and seasonal movements of the turtle Graptemys pulchra (Baur), in Alabama. Bulletin of the Florida Graptemys flavimaculata. Journal of Herpetology 30, 376–385. State Museum. Biological Sciences 21, 47–111. Jones, R.L., in press. Reproduction and nesting of the endangered Shine, R., 1980. ‘‘Costs’’ of reproduction in reptiles. Oecologia 46, , Graptemys oculifera, in Mississippi. 92–100. Chelonian Conservation & Biology. S-Plus, 4.5., 1998. S-Plus 4.5 Standard Ed. Data Analysis Product King, J.M., Heinen, J.T., 2004. An assessment of the behaviors of Div. MathSoft, Inc. Seattle, Washington. overwintering manatees as influenced by interactions with Spotila, J.R., Foley, R.E., Standora, E.A., 1990. Thermoregulation tourists at two sites in central Florida. Biological Conservation and climate space of the slider turtle. In: Gibbons, J.W. (Ed.), 117, 227–234. Life History and Ecology of the Slider Turtle. Smithsonian Lahanas, P.N., 1982. Aspects of the life history of the southern Institution Press, Washington, DC, pp. 288–298. black-knobbed sawback, Graptemys nigrinoda delticola folkerts Stockwell, C.A., Bateman, G.C., Berger, J., 1991. Conflicts in and mount. Master’s thesis, Auburn University, Auburn, national parks: a case study of helicopters and bighorn sheep Alabama. time budgets at the Grand Canyon. Biological Conservation 56, Linck, M.H., DePari, J.A., Butler, B.O., Graham, T.E., 1989. Nesting 317–328. behavior of the turtle, Emydoidea blandingii, in Massachusetts. Swimmer, J., 1997. Physiological consequences of basking, Journal of Herpetology 23, 442–444. disease, and captivity in the green turtle, Chelonia mydas. Moll, D.L., 1974. Notes on the behavior of Isle Royale painted PhD dissertation, University of Michigan, Ann Arbor, turtles (Chrysemys picta belli). Journal of Herpetology 8, 254–255. Michigan. Moore, M.J.C., 2003. Behavioral ecology of the threatened Systat Inc., 1997. Systat for Windows: Statistics. Version 7 Edition. yellow-blotched map turtle, (Graptemys flavimaculata): SPSS Inc., Evanston, IL. implications for conservation and management. Master’s U.S. Fish and Wildlife Service, 1991. Endangered and threatened thesis, Southeastern Louisiana University, Hammond, LA. wildlife and plants: threatened status for the yellow-blotched Pallas, D.C., 1960. Observations on a nesting of the , map turtle, Graptemys flavimaculata. Federal Register 56, Clemmys insculpta. Copeia 1960, 155–156. 1459–1463. Parent, C., Weatherhead, P.J., 2000. Behavioral and life history Vogt, R.C., 1979. Cleaning/feeding symbiosis between grackles responses of eastern massasauga rattlesnakes (Sistrurus (Quiscalus: Icteridae) and map turtles (Graptemys: Emydidae). catenatus) to human disturbance. Oecologia 125, 170–178. Auk 96, 608–609. Parmenter, R.R., 1981. Digestive turnover rates in freshwater Whittow, G.C., Balazs, G.H., 1982. Basking behavior of the turtles: the influence of temperature and body size. Hawaiian green turtle (Chelonia mydas). Pacific Science 36, Comparative Biochemistry and Physiology 70A, 235–238. 129–139.