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«THE TRIALS OF MOTHERHOOD: MATERNAL BEHAVIOR PATTERNS AND ANTIPREDATOR TACTICS IN THOMSON’S GAZELLE (GAZELLA THOMSONII), A HIDING UNGULATE Blair A. ...»

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THE TRIALS OF MOTHERHOOD:

MATERNAL BEHAVIOR PATTERNS AND ANTIPREDATOR TACTICS

IN THOMSON’S GAZELLE (GAZELLA THOMSONII),

A HIDING UNGULATE

Blair A. Roberts

A DISSERTATION

PRESENTED TO THE FACULTY

OF PRINCETON UNIVERSITY

IN CANDIDACY FOR THE DEGREE

OF DOCTOR OF PHILOSOPHY

RECOMMENDED FOR ACCEPTANCE

BY THE DEPARTMENT OF

ECOLOGY AND EVOLUTIONARY BIOLOGY

Adviser: Daniel I. Rubenstein January 2014 © Blair Allison Roberts, 2014. All rights reserved.

For my parents, without whose investment I would surely have fallen to the jackals.

iii Abstract This dissertation examines risk management tactics of female Thomson’s gazelles during the early stages of motherhood, when fawns experience high predation risk. Fawns’ main defense is the hiding strategy, in which they spend long periods of time concealed in vegetation apart from their mothers. Hiding requires maternal cooperation and has the potential to affect maternal risk and behavioral patterns.

Immediately following birth, the fawn is unable to hide. Avoidance of fawn predation depends on the social and environmental contexts of parturition. Most mothers either isolate from conspecifics and give birth in tall grass or remain in social groups and give birth in short grass. The latter tactic provides greater protection from conventional predators, but pressures such as conspecific harassment may lead mothers to give birth in isolation. Both tactics improve neonates’ survival probability compared to behavior that is inconsistent with either tactic.

Once hiding begins, fawns are concealed and relatively safe from detection by predators, and mother-fawn interactions are limited to brief active periods. This framework affords mothers the freedom to schedule investment behaviors and minimize the impact of motherhood on their activity. Peaks in maternal vigilance precede and coincide with active periods, when fawns are at greatest risk. Outside of active periods, mothers are able to behave identically to non-mothers.

As fawns transition out of the hiding strategy, they increase their exposure to predators.

More frequent activity periods enable fawns to move hiding spots more often, which allows mothers to track group movements more effectively. Mothers and fawns rely on increased time spent in social groups and in short grass habitats to mitigate the increase in fawn risk. Thus, as fawns transition out of hiding, mothers transition back to normal activity, grouping, and habitat use patterns.

–  –  –

experiment involving simulated predator attacks, we found that mothers do not rely on group vigilance to detect potential fawn predators, that they exhibit riskier responses than non-mothers, and that the presence of a mother in a group can affect the group’s response in ways that may reduce maternal risk.

–  –  –

I am lucky to have called Princeton my home for the last five and a half years, and as beautiful as the place is, it’s the people in it that have made it such an engaging environment.

First, I thank my advisor, Dan Rubenstein, for all of the support he has provided over my graduate career. Beginning with my first trip to Kenya in the summer before I started at Princeton and continuing through the stressful writing process, Dan has been instructive and encouraging while still allowing me a great deal of independence in conducting my research.

I also thank my committee members, Henry Horn, Jeanne Altmann, and Jim Gould, for their instruction and support throughout my graduate career. Siobhan Condran, Lolly O’Brien, the late Amy Bordvik, and Richard Smith have all been helpful in managing the logistics of being a grad student and EEB department member.

I am grateful to my fellow Rubenstein lab members and cohort-mates for their feedback and support: Corinne Kendall, Cassandra Nuñez, Jenny Schieltz, Caitlin Barale, Ipek Kulahci, Eili Klein, Stephanie Hauck, Qing Cao, Adrienne Tecza, Nitin Sekar, Molly Schumer, and Chaitanya Yarlagadda. The graduate student community is one of EEB’s greatest assets, and I am happy to count many of my colleagues as friends as well. Thanks especially to Sam Rabin, Ann Tate, Carey Nadell, Caroline Farrior, Andrew Hartnett, Jim Adelman, and Carla Staver for many good times at trivia, on the softball field, at football days and at the holiday party.

Since 2008 I have made six trips to the field totaling more than sixteen months, and Laikipia has come to feel a lot like my second home. I am grateful to the Government of Kenya for granting me permission to work in such a breathtaking environment, to Mpala Research Center for serving as my home base for my first visits and for providing logistic support thereafter, and to Ol Pejeta Conservancy for allowing me to live and work on the premises. Special thanks to

–  –  –

management and Ecological Monitoring department, especially Nathan Gichohi and Martin Mulama. Through their tireless efforts, the Ol Pejeta Research Center staff – Kosgei, Erick, Emily, Monica and especially Catherine Mundia – truly made a converted stable feel like home.





I thank them as well as the numerous security guards that assisted with tedious vegetation work while protecting me from buffalo and other beasts.

The research center got lonely at times, so I am grateful for the friendships and memories I formed with other residents – especially Kim Vanderwaal, Nicole Sharpe, Jenny Schieltz, and George Paul. You are the stars in the rotating cast of amazing and interesting people that made up my field family.

I owe thanks to my family, whose influence began long before graduate school and will continue long after. My siblings – Tadd, Paige, Brooke and Dane – were the subjects of my first dabblings in the study of the behavior of wild animals. Thanks to Kathy and Kate for many fantastic weekend escapes full of wine and food in Long Valley and Old Lyme. And of course, thanks to my parents. I remember a day when I was very young and had just sorted out that the “junior high”, “high school”, and “college” mentioned in the TV shows I was watching referred to various stages of education that still lay ahead of me. After verifying this with my mother, I asked if after college was when I would finally have a job, to which she replied, “No, after college you’ll probably go to grad school.” That grad school did in fact follow after college is as much as a result of my own motivation and hard work as my parents’ unending encouragement. I am so happy to have been able to travel with them in Kenya and share with them what they have enabled me to accomplish.

Finally, I thank Mike, my best friend and soon-to-be husband. His patience, love and

–  –  –

2012 as the happiest day.

Financial support for this research came from Princeton University, the Department of Ecology and Evolutionary Biology, the Philadelphia Chapter of the Explorers Club, the Animal Behavior Society Student Research Grant program, the American Society of Mammalogists Student Travel Grant program, and the Dean’s Fund for Scholarly Travel.

–  –  –

Blair A. Roberts Parenthood is a study in balance and compromise. Prior to reproduction, an individual’s mission is to survive long enough to create offspring. Once this is accomplished, the parent is

faced with a series of decisions that carry serious repercussions for its reproductive success:

should the parent care for its young? If so, what proportion of available resources should it commit to its offspring? How much should it keep in reserve for its own survival and future reproductive efforts? The parent’s answers to these questions are invariably affected by many factors, including the current social and environmental contexts, qualities of the offspring, and characteristics of the parent itself. In this thesis, I examine the interplay between motherhood and risk in Thomson’s gazelle (Gazella thomsonii), a small African ungulate species. I explore the tactics mothers use to protect their offspring, variation in maternal strategies, and the effects these behaviors have on mothers themselves.

Parental investment Parental care is one means by which individuals may increase their reproductive success. By spending time and energy provisioning or protecting young, parents can improve their offsprings’ chance of survival and thereby increase the abundance of their own genes in the next generation.

However, such parental investment in one offspring reduces the parent’s ability to invest in its

other offspring (Trivers 1972). For iteroparous parents, the costs of investment take two forms:

fecundity costs occur when the parent’s ability to produce or care for offspring is hindered by a depletion of bodily resources, whereas survival costs result from the parent perishing before its next reproductive opportunity (Bell 1980). In determining the appropriate amount of investment for a given offspring, parents must weigh both the likely pay-off and the potential costs.

The desired benefit to the parent of any investment is an increase in inclusive fitness resulting from the improved chance that the offspring will survive and reproduce. Parental investment is expected to increase with the offspring’s reproductive value (Clutton-Brock 1991).

Reproductive value is a combination of the offspring’s probability of surviving to reproductive age and its reproductive potential, or the proportion of the parent’s genes that the offspring is likely to pass on to subsequent generations. For example, older or larger offspring may be more likely to survive to reproductive age and thus represent a greater probability of increasing the parent’s inclusive fitness (Tessier & Consolatti 1989; Svagelj et al. 2012). Likewise, in many species, reproductive potential varies with offspring sex, resulting in higher investment in offspring of one sex over the other (Clutton-Brock et al. 1981; Trillmich 1986; Bercovitch et al.

2000). Reproductive value can also vary with other offspring characteristics, such as brood size (Coleman & Fischer 2010; Teichert et al. 2013), health (Saino et al. 2000), and birth or laying date (Redmon et al. 2009; Kivanova et al. 2011).

The value of a parent’s investment also depends on the relative contribution the investment makes to the offspring’s survival and reproductive success. The reward of investing to the parent is large if the offspring is unlikely to survive or reproduce without the investment, and is small if the offspring has a high probability of success without parental assistance or if the offspring is unlikely to survive even with large amounts of investment. These concepts often play out in parental defense of offspring, where parents are more likely to defend or defend more vigorously when offspring are more able to capitalize on defense efforts by escaping (Redondo & Carranza 1989), or when the offspring are likely to die without parental intervention (the “harm to offspring” hypothesis; Koskela et al. 2000; Goubault et al. 2007).

As described above, the cost to the parent of an investment in current offspring is a reduced capacity for investment in future offspring. All else being equal, a parent’s investment should decrease as costs and risks to their future reproduction rise. Reductions in investment are commonly seen when resource availability is low or parental body condition is poor (Drent & Daan 1980; Smith 1987; Scott & Traniello 1990; Smith & Wootton 1995). Under these circumstances, parental expenditures are more likely to negatively affect future reproductive opportunities or the survival of the parent. It is often difficult to determine whether observed reductions in care result from adaptive decisions by parents or are simply the unavoidable consequences of low resource availability (Clutton-Brock 1991). However, some studies have successfully separated these two drivers and demonstrated that parents do indeed exercise control over care levels by adjusting their investment strategies in response to surrounding conditions (e.g.

Festa-Bianchet & Jorgenson 1998).

Parents should weight the benefits and costs described above according to their own relative reproductive value compared to that of their offspring. Generally, parents’ reproductive value diminishes with age as the parents’ expected number of future reproductive opportunities dwindles. Therefore, as parents age they should increase investment in the offspring at hand rather than saving up for opportunities that may never come (the “terminal investment hypothesis”; Clutton-Brock 1984). Increases in parental investment with age have been demonstrated across taxa (e.g. Pugesek 1983; Bercovitch et al. 2009; Hoffman et al. 2010; Heinze & Schrempf 2012).

Ungulates: antipredator behavior and offspring care Ungulates are a diverse and widespread group, numbering over 450 species (Groves & Grubb 2011) and inhabiting most of the world’s terrestrial ecosystems. In these systems they play a variety of ecological roles, including serving as common prey items for many predator species.

Young ungulates are particularly vulnerable due to their smaller size. Infant mortality rates of 50% or more are common in ungulate populations, and where predators are present, predation is usually the primary cause of infant death (Estes & Estes 1979; Linnell et al. 1995; Janermo 2004;

Lomas & Bender 2007). This pressure has selected for a variety of behaviors designed to mitigate predation risk in both adults and their offspring.



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