Parturition Effects on Sociality and Dynamic Interactions of Female White-tailed Deer

doi:10.21203/rs.3.rs-3352719/v1

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Parturition Effects on Sociality and Dynamic Interactions of Female White-tailed Deer

https://doi.org/10.21203/rs.3.rs-3352719/v1

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Background

Female white-tailed deer (Odocoileus virginianus) typically form matriarchal social groups throughout much of the year; however, little research has examined the effect of parturition on sociality. We used measures of dynamic interaction, a function of travel direction and displacement, to examine social interactions between adult females before and after parturition. We monitored parturient, free-ranging individuals on a 126-ha property using vaginal implant transmitters linked to GPS collars during a 2-month period surrounding peak parturition (1 May–30 June 2016). We calculated local dynamic interaction (di; cohesiveness of movement for each time step) and global dynamic interaction (DI; cohesiveness of movement throughout the study period) metrics for all female pairs with overlapping 95% kernel density home range estimates (n = 29 interaction pairings).

Results

Global DI was correlated positively with home range overlap (%). Mean local di values indicated moderate social cohesion within the population prior to parturition. Following parturition, mean local di values declined below zero suggesting avoidance among female pairs with overlapping ranges. Mean local di began to increase approximately 15 days postpartum but did not return to prepartum levels during our study period (~ 25 days postpartum).

Conclusions

The changes in female social dynamics following parturition are likely a trade-off among several factors such as neonate mobility, predator avoidance, and nutritional demands. However, the trends we observed are to be expected given the life history of female deer around parturition in which sociality declines around parturition and then returns gradually to pre-parturition levels.

dynamic interaction

Odocoileus virginianus

parturition

social behavior

spatial ecology

white-tailed deer

Social dynamics of female white-tailed deer (Odocoileus virginianus) center on matrilineal groupings of related individuals [1, 2] where individuals within social groups have extensive range overlap and demonstrate similar use of the landscape [3, 4, 5]. Group sociality among females is strong and persist throughout much of the year, and membership within a social group allows individuals to maximize time spent foraging by reducing individual vigilance [6, 7, 8] However, there are periods during the year when reduced sociality of female deer is expected such as around parturition when females seek solitude for giving birth [9, 10].

During and after parturition, social group dynamics appear to be disrupted such that home ranges become smaller, daily movement rates decrease, resource use is shifted, and the frequency of association with other individuals is reduced [9, 10, 11, 12, 13]. Social isolation and agnostic behavior around the timing of parturition may be an adaptive strategy to reduce both competition for food resources among the dams and predation risk for the neonates. Lactation is more energetically costly than gestation [14]. Neonate survival rates vary as a function of a dam’s access to quality nutrition [15, 16], suggesting social group disruption may relate to the defense of quality food resources. Furthermore, white-tailed deer neonates utilize a fear bradycardia hider strategy in response to predation risk [17, 18], where the neonate will remain hidden and not flee when approached by a predator. Social disruption and a dispersion of female activity may prevent predators from identifying large social groupings and potential locations of hiding neonates.

Social dynamics within white-tailed deer groups have important implications for population demographics, dispersal behavior, and management [3, 19, 20], but have historically been difficult to measure. Quantifying the timing and extent of shifts in social dynamics requires several monitored individuals with known social relationships, typically within a relatively small geographical area. Previous research has primarily relied on captive populations [9, 10, 21] to overcome these considerations. Furthermore, previous research has confirmed that female social interactions are altered around the timing of parturition but utilized static metrics when quantifying interactions, such as spatial proximity or the proportion of home range overlap [9, 10, 22]. More recent analytical methods calculate dynamic interactions, a measure of the inter-dependency and association of movements between individuals [23, 24, 25]. While measures of dynamic interaction better utilize fine-scale GPS data to understand how the movements of animals are related [22, 26] a paucity of research exists using these emerging analytical methods to examine finer-scale effects of parturition on female sociality in free-ranging populations of white-tailed deer.

Our objective was to quantify the extent and timing of social disruption within a free-ranging population adult female white-tailed deer before and after parturition. Specifically, we assessed the correlation between measures of social dynamic interaction and a measure of static interaction (home range overlap). Furthermore, we used a time-series analysis to examine how measures of dynamic interaction changed within the population throughout the parturition period. We hypothesize that (1) measures of social dynamic interaction among adult female white-tailed deer will be positively corelated with a measure of static interaction, (2) dynamic interaction measures among females will immediately and markedly decrease following parturition, and (3) measures of dynamic interaction among females will remain low while dams rear their offspring, at least until fawns become more mobile.

Study area

The study was performed on a 126-ha section of contiguous private property in south-central Sussex County, Delaware, USA (38.49410°N, 75.42788°W; Fig. 1). The study site was 27% forest, 31% agriculture, 39% shrubby wetland, and 3% wildlife plantings split evenly between Brassica spp. and clover (Trifolium spp). A 65-ha section of the site was enrolled in the U.S. Department of Agriculture (USDA) Wetland Reserve Program and occasionally inundated with pockets of saturated soils or standing water. During the study period, the agricultural areas were planted in either soybeans or corn, the 2 most common agricultural crops in Sussex County [27]. The 15-year average (2006–2020) for daily temperatures in Sussex County ranged from − 0.7°C to 9.1°C in January and 19.6°C to 30.1°C in July (Georgetown; [28]). Annual precipitation in Sussex County averaged 112 cm (2006–2020, Georgetown; [28]). The deer density in Sussex County was 19.4 deer/km² [29]. The white-tailed deer breeding season occurred primarily between the last week of October and first week of December, with a mean conception date of 15 November [Delaware Division of Fish and Wildlife, unpublished data]. The mean date of parturition in Sussex County was 28 May [30], and most neonates (57%) were born during a 12-day period (26 May–5 June) [Delaware Division of Fish and Wildlife, unpublished data].

Deer capture and monitoring

We captured deer from 15 December 2015 to 31 March 2016 via drop net and rocket net [31]. We sedated all captured deer using an intramuscular injection of xylazine (0.5 mg/kg) and placed a blindfold over the eyes of each deer to minimize stress. Each deer received two self-piercing numbered metal ear tags (Model 1005-49; National Band and Tag Company, Newport, Kentucky, USA) and 2 white plastic button cattle tags (3 cm diameter) with black numbers (Allflex USA, Dallas, Texas, USA). We aged deer using tooth replacement and wear [32] and fitted all females ≥ 1.5 years of age with an iridium GPS collar (model G2110E2, 800g, Advanced Telemetry Systems, Isanti, Minnesota) and a vaginal implant transmitter (model M3930U, 23g, Advanced Telemetry Systems, Isanti, Minnesota) linked to the collar via ultra-high frequency radiotelemetry (rVIT) [33]. We followed established guidelines for rVIT deployment [34, 35] and inserted transmitters to a depth of 20 cm. We monitored animal condition and vital signs (i.e., temperature [°C], heart rate, and respiration) until individuals left the capture site under their own power. We followed the guidelines of the American Society of Mammalogists for mammal care and use [36]; the University of Delaware Institutional Animal Care and Use Committee approved all trapping and handling procedures (protocol #1288).

Analysis of dynamic interactions

We programmed GPS collars to record 1 location/hour from 1 May to 30 June; a 2-month period approximately centered on the peak date of parturition (28 May) [30]. We removed all unrealistic location fixes but did not censor locations using dilution of precision error screening [37] because landscape characteristics associated with location bias, such as rugged topography and heavy canopy cover [38, 39, 40], were not typical within the study area.

For each individual, we generated a 95% isopleth home range during the 2-month study period using kernel density estimation in package adehabitatHR in program R [41]. For all subsequent analyses, we calculated social interaction metrics only among females that had overlap between their 95% isopleth home ranges (interaction pairings); thus, we assumed females with non-overlapping ranges were not socializing during the parturition period. We calculated home range overlap as a percentage, such that the total area (ha) of range overlap was divided by the area of the merged home ranges for each interaction pairing and multiplied by 100 (Fig. 2) [2].

We used the package wildlifeDI in program R [25, 26, 42] to generate measures of dynamic interaction for each social pairing, including global dynamic interaction (DI) and local dynamic interaction (di) values. Dynamic interaction values generated by the wildlifeDI package are a function of the directionality and displacement of movement trajectories for paired animals over the same period. Values range from − 1 to 1, with positive values associated with interactive or socially correlated movements, negative values associated with repulsion or social avoidance, and 0 indicating no association [25]. Global DI is a single metric calculated for each interaction pairing reflecting the relatedness of movements for the duration of a study period or subperiod, while local di values are generated in a time series and correspond to each path segment (step) of the interaction pairing [25, 42].

Table 1

Identification number, age, home range size (ha), and date of parturition, for 10 adult female white-tailed deer tracked in Sussex County, Delaware from 1 May to 30 June 2016. Home range overlap (%) is shown between each pair of individuals.
ID	Age Estimate	Home Range Size (ha)^a	Parturition Date	Home Range Overlap (%)
ID	Age Estimate	Home Range Size (ha)^a	Parturition Date	720	751	753	762	770	783	785	786	800
621	5	55.3	17 May	0.0	0.0	0.0	0.0	28.8	0.0	0.0	0.0	10.0
720	4	67.8	09 May		3.7	0.0	23.3	21.5	7.6	52.6	58.9	10.9
751	2	28.8	23 May			9.5	23.0	0.0	5.1	1.1	6.9	0.0
753	5	26.8	22 May				0.0	0.0	16.9	0.0	0.0	0.0
762	5	36.3	31 May					1.4	3.2	18.4	33.1	0.0
770	4	69.2	26 May						4.2	23.6	11.6	30.3
783	3	42.4	20 May							8.1	6.5	3.2
785	2	56.3	27 May								34.3	6.7
786	4	69.5	02 June									5.0
800	3	39.0	27 May
^a Calculated 1 May–30 June using 95% Kernel Density Estimation

We evaluated the relationship between home range overlap (%) and global DI values for each interaction pairing using a generalized additive model in package ‘mgcv” in Program R [43]. We established the hour of parturition for each female using the timestamp on the remote notification of a photosensor trigger for the rVIT [33] and set the hour of parturition equal to the time of the subsequent hourly fix (e.g., notification of a photosensor trigger event timestamped at 08:37 resulted in an 09:00 hour of parturition). We centered the mean local di values for all interaction pairings on the hour of the first parturition event within each respective pairing, such that the hour of the first parturition event was set to a value of 0. Next, we examined the change in local di values throughout the parturition period by averaging the local di values for all interaction pairings at each hourly time step. We then plot the mean local di values throughout the parturition period as a function of the number of hours since the first parturition event. All means are reported ± SE.

We captured and placed GPS collars on 10 adult females who subsequently birthed fawns during the study period, resulting in 13,838 location fixes (97% fix success rate) during the 2-month study period. Parturition ranged from 09 May to 02 June, with a mean date of 24 May (Table 1). Mean home range size during the study period was 49.1 (± 5.2) ha. We identified 29 interaction pairings based on home range overlap (Table 1). Average home range overlap between all pairings, even those without any overlap, was 10.4% (± 2.1), whereas home range overlap considering only deer with overlap > 0% was 14.9% (± 2.8).

Considering only pairings with home range overlap, global DI values among interaction pairings ranged from − 0.03 to 0.28 (\(\stackrel{-}{x}\) = 0.13 ± 0.02) and were correlated positively with the percentage of home range overlap between the same pairwise set of females (F = 6.01, residual df = 26.03, P = 0.005; Fig. 3). Mean local di values as a function of hours since parturition ranged from 0.17 to 0.27 during the 200-hour period preceding the first parturition event (Fig. 4). Immediately following the first parturition event (at time zero), mean local di values began to steadily decrease from 0.26 for a period of 356 hours (14.8 days) to -0.03 (Fig. 4). After reaching the lowest local di level (at 356 hours postpartum), the following ~ 250 hours involved a steady increase in local di; however, during these 250 hours, local di did not return to prepartum levels before the end of the study period.

These results support earlier findings that social behavior and proximity among female white-tailed deer are affected by timing of parturition, whereby social behavior and interactions decrease starting at parturition [9, 10, 11]. Despite similar findings with other studies that used observational or static spatial overlap indices, our results provide more quantitative metrics to how similar movement is between pairs of female white-tailed deer. Since most early studies used static spatial overlap metrics to assess changes in social behavior and herd dynamics, we examined the correlation between home range overlap and measures of dynamic interaction. The positive correlation between percentage of home range overlap and global DI supports the hypothesis that static spatial overlap is an approximate method to track changes in spatial behavior among individuals. However, static measures of interaction are not reliable indices of relatedness, social group membership [2], actual contact, or cohesive movement [26]. Our study also had the added benefit of knowing the exact timing of parturition given the use of rVITs; most early studies relied on visual observations or predicted parturition from estimated conception dates [11, 44].

The consistent and gradual decline in mean local di following parturition was unexpected given past literature indicating that social interactions among female herd members virtually cease to exist until the fawn becomes more mobile [9, 21]. We expected population mean local di values to reflect a more abrupt disruption of female social dynamics after parturition to reduce predation risk effects, which is partially mitigated by solitude seeking and hiding of the newborn in smaller areas with fewer deer [10, 45]. Another consideration for the gradual decline in social interactions may be driven by methodological reasons, at least partially. We centered local di values for each interaction pairing on the hour for the first of 2 parturition events, so the more gradual decline in mean local di may reflect a short period where socially agonistic behaviors are only present in 1 member of each pairing because the other individual has yet to give birth. Despite agonistic behaviors from the parturient female, other collared females may exhibit spatiotemporal use of similar ranges; therefore, we still would document a potential interaction. It also is likely that individuals may interact during foraging bouts while the newborn remains hidden. Another study corroborates this hypothesis in that movement distance of female elk (Cervus canadensis) showed a similar pattern of decline after parturition, indicating that movement of the dam is still persistent albeit at a lower rate [44], so we expect female-female interactions to decline in relation to reduced movement.

Alternatively, the prolonged decline in mean local di values may accurately reflect a reduction in social tolerance and group cohesion which may be less immediate than we had hypothesized. If the energetic demands of lactation are driving the disruption of social dynamics, and those energetic demands accrue constantly throughout the summer, a steadier decline in social tolerance would be expected. Furthermore, declining social tolerance at the population level may be continuously offset as neonates die and dams without fawns return to prepartum levels of sociality [10]. While our sample size of individual females was limited, all dams in our study had at least 1 neonate survive beyond 1 week and 7 of 10 had at least 1 neonate survive to 2 weeks, suggesting the movement behavior of dams following the loss of their neonates was not a major factor in the prolonged decline of mean local di we observed.

Previous research reported the reduced sociability in captive females during lactation persisted for up to 12-weeks postpartum [10]. Ozoga et al. [9] similarly reported reduced levels of social group affiliation for up to 3 months postpartum in a captive population, but claimed territorial behavior ceased after 4 weeks. While our monitoring period only extended ~ 25 days postpartum, we observed a noticeable inflection point at ~ 14.8 days, where values of population mean local di began to increase following a period of steady decline. Although behaviors associated with the hider strategy among neonates may persist for up to 60 days, a transition to the neonate following the dam is not a discrete behavioral event [46]. Neonates become more agile with age and will begin to flee from predators at approximately 2 weeks old [47, 48, 49], and 2 weeks has also been proposed as the time needed to establish the dam-neonate bond [21]. Although the energetic demand of lactation persists well into the summer, the increasing mobility and agility of the neonates progressively reduces the risk of predation when traveling with the dam. Such a transition may allow a shift in the behaviors of the dam, whereas the benefit of shared group vigilance may begin to gradually outweigh the benefit of social isolation and predator avoidance. Similarly, Nixon et al. [50] reported a general increase in tolerance of other deer among dams 2–3 weeks postpartum in Illinois. Nixon et al. [50] also noted the reformation of female social groups progressed as a function of relatedness, such that dams began to tolerate social interactions with closely related females more readily than distantly or unrelated individuals following the 2–3-week postpartum period. Our observation of increasing mean local di values between 15–25 days postpartum may reflect a period of social reintegration among females, which are likely related [2, 3].

Additionally, agonistic social cues from adult females have been proposed as a proximate motivating factor for spring dispersal among juveniles of both sexes [19]. The ~ 15-day period of decreasing local di values observed corresponds directly to the peak of spring dispersal movements among juveniles in both Sussex County [51] and the broader region [52]. A relatively shorter period of heightened social aggression among related females may reduce the probability a juvenile female will disperse during the spring, which would in turn facilitate the maintenance of matrilineal groups.

A necessary caveat to our research is the limited geographic scope and sample size of our population. Because there is often a disparity in the social and spatial behaviors demonstrated by captive white-tailed deer [45, 53, 54], our objective required a free-ranging population. A sufficient sample size of interaction pairings of parturient females with precisely known parturition times would be logistically difficult over a large geographic area, and these spatial limitations were necessary given our research objective. Additionally, white-tailed deer demonstrate a great degree of behavioral plasticity across their range. Social isolation and agnostic behaviors are likely more prominent in populations with relatively concise conception and parturition periods. When parturition occurs over a relatively long period, as is the case in regions of the southeastern United States [45], periods of social agonism and aggression may be less pronounced. Our results, and the results of future research into deer social dynamics, should be interpreted within the context of regional variability in habitat and population demographics.

While more static rates of spatial proximity, contact, and range overlap may reflect similar use of space among individuals, they do not necessarily represent social interactions or group membership. Measures of dynamic interaction appear to reflect both social associations and the seasonal changes in social dynamics within a free-ranging population of white-tailed deer, and we recommend their use when assessing social interactions and group membership. Our results suggest postpartum social dynamics do not follow a series of discrete behavioral periods but rather a continuous gradient of progressive isolation followed by a gradual reformation of social dynamics. We caution against using discrete temporal categories relating to social behavior (e.g., hider phase, follower phase) to delineate periods of movement behaviors in adult females or periods of demographic responses in neonates; rather, we suggest analyzing data in a more continuous fashion, which will reveal subtle changes or thresholds in the movement response.

local dynamic interaction

global dynamic interaction

GPS

global positioning system

NOAA

National Oceanic and Atmospheric Administration

rVIT

radio-linked vaginal implant transmitter

USDA

United States Department of Agriculture

Ethics approval

Animal handling procedures were approved by the University of Delaware Institutional Animal Care and Use Committee under permit #1288.

Consent for publication

Not applicable.

Availability of data and materials

Data used for the analyses described in the manuscript are available from the authors upon reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

The Wildlife and Sportfish Restoration grant from the United States Fish and Wildlife Services under award number F15AF00929 and the Delaware Department of Natural Resources and Environmental Control provided major funding for this research. The U.S. Department of Agriculture National Institute of Food and Agriculture, Hatch project DEL00712 and McIntire Stennis DEL00672, also supported this work.

Authors Contribution

JB and JR secured research funding. JH, JB, and SW conceived the research objectives and experimental design. JH and JD collected field data, JH analyzed the data and drafted the manuscript with input from all co-authors. All authors read and approved the final manuscript.

Acknowledgments

We are grateful to Kevin Lamp, Andew Orlando, Miranda Reinson, and numerous technicians for assistance with deer capture and data collection. We thank landowner Nathan Hudson for granting permission to access the study property.

Authors’ information

JH is an assistant professor in the wildlife biology program at Bemidji State University, JD is an assistant big game biologist with the Oregon Department of Fish and Wildlife, SW is a research assistant professor in the Texas A&M Natural Resources Institute, and Department of Rangeland, Wildlife and Fisheries Management at Texas A&M University, JR is a program manager for species conservation and research with the Delaware Division of Fish and Wildlife, and JB is a professor and department chair in the entomology and wildlife ecology department at the University of Delaware.

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No competing interests reported.

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Parturition Effects on Sociality and Dynamic Interactions of Female White-tailed Deer

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BACKGROUND

METHODS

Study area

Deer capture and monitoring

Analysis of dynamic interactions

RESULTS

DISCUSSION

CONCLUSIONS

List Of Abbreviations

Declarations

References

Additional Declarations

Status:

Version 1