Data Collection Methods Used in Primatology Research Paper Purpose The purpose of this activity is to allow you to apply the knowledge you have gained abo

Data Collection Methods Used in Primatology Research Paper Purpose

The purpose of this activity is to allow you to apply the knowledge you have gained about data collection methods used in primatology from the previous pages. For this activity, you will find a published research article on any non-human primate species, and identify what method(s) they used to collect data. Insofar as you are able, try to identify why those methods were used (indeed, some authors may say why they selected their methods). If they do not explain their choice of methods, based on what you learned about data collection, try to name why you think they chose those particular methods. Lastly, share the link to the research article. This activity will help ensure that you can describe different methods of gathering in data biological anthropology, which will help us meet Course Learning Objective #3, which is to evaluate ethical issues related to different types of anthropological data (on humans and non-human primates).

Skills

This activity will help you practice the following skill:

Module-level objective 3.1: You will be able to describe some methods of gathering data in biological anthropology.
Tasks
Choose an original research article published on any non-human primate species.
Identify and explain the method(s) used by the authors (behavioral and/or biological sample collection). Do not be alarmed if they used methods that we did not discuss in these modules – there are many methods in primatology – just do your best!
Attempt to explain why the authors may have chosen the method(s) they used. If you get lucky, the authors may explain in the article! Received: 6 February 2017
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Revised: 19 October 2017
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Accepted: 23 October 2017
DOI: 10.1002/ajp.22724
RESEARCH ARTICLE
“Stink flirting” in ring-tailed lemurs (Lemur catta): Male
olfactory displays to females as honest, costly signals
Amber D. Walker-Bolton1
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Joyce A. Parga2
1 Department
of Anthropology, University of
Toronto, Ontario, Canada
Sexual selection for honest behavioral displays of quality has driven the development
2 Department
of Anthropology, California
State University, Los Angeles, California
of remarkably complex courtship behavior in many animal species. Olfactory displays
Correspondence
Amber D. Walker-Bolton, Department of
Anthropology, University of Toronto, 19
Russell Street, Toronto, Ontario M5S 2S2,
Canada,
Email: amber.walker.bolton@mail.utoronto.ca
Ring-tailed lemur (Lemur catta) scent marking of substrates has been studied
are often overlooked as an area of inquiry compared to auditory and visual displays.
extensively, although the male olfactory displays of anointing and wafting tails to
females has received relatively little attention. We studied the role of male olfactory
displays to females, evaluating whether such signals function as honest, costly signals
of male dominance status in two groups of wild L. catta at Berenty Reserve,
Funding information
Roehampton University Scholarship; L.S.B.
Leakey Trust Grant; Roehampton University
Sacred Heart Scholarship
Madagascar. Our results suggest that male tail anointing and tail wafting displays to
pre-estrous and estrous females are correlated with male dominance rank, and
moreover appear to operate as costly signals, as such displays increase aggression
received from males and females while other types of scent marking do not.
Furthermore, females showed greater mating preference (as measured by sexual
presents) for resident males who performed the “anoint tail” and “waft tail” displays
towards them. When males perform the “anoint tail” and “waft tail” displays to females,
they receive higher levels of aggression than if they were to perform other types of
scent marking. Interestingly, immigrating (peripheral) males performed the “anoint tail”
and “waft tail” displays at higher rates than resident males, which could honestly
indicate their quality or may simply be associated with the alternative mating strategy
of transferring between groups to gain mating opportunities. Our finding that tail
anointing and tail wafting displays function as honest signals of dominance for resident
males—and that these costly displays appear to positively affect female mate choice—is
the first evidence of this function for this particular olfactory signal in L. catta.
KEYWORDS
courtship, dominance, honest signaling, scent marking, sexual selection
1 | INTRODUCTION
immigrating males. Elaborate male ornaments and associated behavioral displays (signals) are important aspects of male sexual communi-
Male ring-tailed lemurs (Lemur catta) anoint and waft their tails to
cation to females because they can convey information on male quality
females in scent displays. In this study, we assess whether tail
to female receivers. Here we are referring to “quality” in the classic
anointing and wafting displays operate as honest behavioral displays of
sexual selection sense of the term sensu (Andersson, 1994); we expect
dominance status. We test whether signaling rates are associated with
that a male’s quality should be related to his dominance status. For a
dominance rank and mating success in resident males, and also
male display to remain honest, there must be an element of risk or
evaluate olfactory signaling and the potential for mating success by
energy expenditure involved which imposes a cost on performing the
Am J Primatol. 2017;79:e22724
https://doi.org/10.1002/ajp.22724
wileyonlinelibrary.com/journal/ajp
© 2017 Wiley Periodicals, Inc.
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display (Grafen, 1990; Zahavi, 1975). Examinations of male costly
the receiving female, often in close proximity and often the female will
displays often focus on visual or auditory communication; until
maintain eye contact with the signaling male. Male tail anointing and
recently, olfactory signaling has been largely ignored (Müller-
wafting to females may perform a sexual monitoring function, as males
Schwarze, 2006). Substantial empirical evidence suggests that
often precede genital sniffing and licking with tail anointing and
chemical communication operates according to predictions of sexual
wafting displays (Jolly, 1967; Sauther, 1991). Gould (1994) suggests
selection theory to facilitate mate choice (Johansson & Jones, 2007).
that male tail anointing and wafting to females is a submissive display in
In primates, strepsirhines are obvious choices when investigating
which the male tests the female’s willingness for a close approach and
olfaction (delBarco-Trillo & Drea, 2014; delBarco-Trillo, Sacha, Dubay,
potential affiliative behavior. Male tail anointing and wafting displays
& Drea, 2012) and whether olfactory signals are potentially costly
towards female recipients have also been described as male sexual
honest indicators of male quality. Among strepsirhines, olfaction has
advances towards females (Pereira & Kappeler, 1997). Male tail
long been known to operate as an important sensory modality in
anointing and wafting displays are multi-modal, because the anointing
L. catta (Martin, 1990; Schilling, 1979), a seasonally breeding, female
and wafting is highly visible, and the scent which is anointed and
philopatric species that lives in large social groups having several males
wafted towards the male or female receiver also sends an olfactory
and females (Jolly, 1966; Sauther, Sussman, & Gould, 1999; Sussman,
signal. Multimodal displays increase the likelihood that a message will
1991, 1992). Scent marking in this species can function as a visual,
be received by the intended recipient (Palagi & Norscia, 2009).
auditory and olfactory display, and can transmit important social
Although honest olfactory signaling through genital marking by males
information to receivers. Dominance rank in males has been found to
(Charpentier et al., 2008) and females (Boulet, Crawford, Charpentier,
correlate with scent marking frequency among L. catta at the Duke
& Drea, 2010) has been reported in this species, male tail anointing and
Lemur Center (Kappeler, 1990a) and in Berenty, Madagascar
wafting displays towards females have not been investigated to
(Oda, 1999), although Gould and Overdorff (2002) did not find a
determine whether they operate as honest and costly signals that
relationship between male dominance rank and rates of scent marking
impact mating outcomes.
among L. catta at Bezá Mahafaly Special Reserve, Madagascar.
We evaluated two main hypotheses: (1) that the male behavioral
Several indicators suggest that male scent marking in this species
display of olfactory signaling to females via tail anointing and tail
is a sexually selected trait (Charpentier, Boulet, & Drea, 2008). Scent
wafting operates as an honest indicator of dominance status; and (2)
gland morphology is sex-specific in this species, and individuals appear
that males will experience increased aggression from males and
to glean olfactory information on individual heterozygosity, as well as
females as a consequence of scent marking displays directed to
relatedness between themselves and odorant donors from scent
females (which might be expected if the signal is costly). We
(Charpentier, Crawford, Boulet, & Drea, 2010). Sexual dimorphism in
additionally considered whether females showed increased mate
this female-dominant species occurs not in body size (Jolly, 1966;
choice for males who use scent marking displays most frequently, and
Kappeler, 1990b) but in scent gland morphology (Kappeler, 1998;
assessed whether the scent marking behavior of resident and
Mertl, 1977; Montagna & Yun, 1962). In addition to the genital glands
immigrating males was associated with mating success.
of both sexes that are used for genitally marking substrates, males have
two specialized scent glands on their pectorals and wrists known as
brachial and antebrachial glands (Hill, 1953; Montagna & Yun, 1962;
Scordato & Drea, 2007). Each of these glands produces a specific and
distinct secretion (Drea & Scordato, 2008) that is used differentially in
2 | METHO DS
2.1 | Study subjects and location
complex, multi-modal behavioral displays (Drea & Scordato, 2008;
This study was conducted from March–June 2010, a period that
Jolly, 1966). Males often combine secretions from their brachial and
includes the mating season in Berenty Reserve, Madagascar (24°58′S,
antebrachial glands before wrist marking (Evans & Goy, 1968; Mertl,
46°16′E) (Budnitz & Dainis, 1975; Jolly, 1966), a private nature
1976). Wrist marking involves scraping the antebrachial gland and the
preserve in the extreme south of Madagascar (Jolly, Koyama,
keratinized spur on the wrist against a substrate, usually a small branch,
Rasamimanana, Crowley, & Williams, 2006). The population of L.
and impregnating the resulting scratches in the bark with scent
catta for Berenty Reserve was reported as 562 individuals in 2015,
(Epple, 1986; Jolly, 1966; Mertl, 1975, 1977; Schilling, 1974). Males
with the largest average group being found in the Tourist Front
use the same process of often combining antebrachial and brachial
(Foulon et al., 2015). Long term, continuous behavioral research on
gland secretions before anointing their tail with scent and wafting the
the Berenty L. catta population has been conducted since 1989
tail towards a male competitor in “stink fights” (Jolly, 1966; Sussman &
(Koyama et al., 2001).
Richard, 1974). Stink fights are multimodal displays and are an
Two L. catta groups (A1 and C1) having their home ranges within the
aggressive act only when directed towards another male (Gould, 1994;
Tourist Front (Jolly, 2009) were studied. During the study period, A1
Jolly, 1966); this paper focuses on the display of tail anointing and
group consisted of 15 members (six adult males, six adult females, three
wafting when it is performed with a female as the target.
subadults), and C1 group consisted of 10 members (two adult males,
Males will anoint and waft their tails toward female recipients as
four adult females, four subadults). In addition, two adult males (FE and
well as males (Evans & Goy, 1968; Jolly, 1966; Mertl, 1976; Petter,
DF) attempted to immigrate into C1 group during the study period.
1962). When males signal to females in this way, they gaze directly at
Immigrating (transferring) males are defined as males who are
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attempting to enter a new group (Sauther, 1991; Sussman, 1992). Data
markings. During focal samples, all agonistic behaviors between the
on the scent marking behavior of the two immigrating males were
focal and other individuals were recorded. In addition, concurrently
included in all analyses except those in which male dominance rank was
with focal sampling, “all occurrences sampling” (Altmann, 1974) of the
calculated, because the immigrant males did not have reliable
group was conducted, specifically recording all male scent marking
dominance rankings in the group. One immigrating male (FE, Table 1)
olfactory displays towards female and male recipients, along with
was first seen with the group 10 days after observations began, and the
recording any aggressive responses by individuals to the scent marking
second male (DF, Table 1) was first seen with the group approximately
display. It was possible to observe the entire group at once for such
one month after the start of the study. Both males remained with the
sampling, as group sizes in this study were small. Scent marking of
group for the remainder of the study period, and were present when
males included genital marks, wrist marks, wrist to pit, anointing tail to
study females started to enter estrus. In addition to the two males in the
males, wafting tail to males, anointing tail to females, and wafting tail to
process of immigrating into C1 group, two visiting males were observed
females (Gould, 1994; Jolly, 1966; Mertl, 1977). Male tail anointing
near A1 group on a single day, when one of the females in this group was
displays involve rubbing the tail between the ventral surfaces of the
in estrus. Although ad lib data were gathered on these two visiting males
wrists and forearm, and are occasionally preceded by shoulder rubbing
on their single-day visit, they remained near the group for such a short
(wrist to pit). Tail wafting displays involve a male waving his tail over his
time that data on their behaviors were not included in analyses.
head towards another individual. Tail wafting displays are typically
Only data from adults were included in analyses. Adults were
performed by signaling males while standing near (3 m) and gazing at
distinguished from subadults based on body size and level of sexual
their partner (Pereira & Kappeler, 1997). Eye contact with the female
development. Adults were defined as sexually mature individuals of full
receiver is often, but not always, seen (A. Walker-Bolton, personal
adult body size having fully developed genitalia (e.g., descended
observation). The order of animals to be focal sampled was randomly
testicles in males [Pereira, 1993]) and were the only individuals
chosen initially, then determined by which animals had the fewest
observed to engage in sexual behavior during the mating season.
number of focal follows.
Subadults were individuals who had not yet reached adult body size,
The data collection period encompassed females’ first estrus
did not have fully developed genitalia, and did not participate in mating.
cycle of the mating season (Van Horn & Resko, 1977), during which
time all group females asynchronously enter estrus within a period
of 1–3 weeks of one another (Sauther, 1991). The female behavior
2.2 | Data collection and definitions
of sexually presenting to males, which functions as female
We used a Psion Workabout MX to record all behavioral data using
solicitation of male mounting in this species (Parga, 2003; Parga
The Observer 5.0 software, programmed with a personalized
& Henry, 2008), helped to determine the estrus period of each
configuration. The ethogram (see Supplementary file) used was
individual female. When a female entered estrus, focal sampling
adapted from Pereira and Kappeler (1997). A.W-B. conducted
was suspended to observe the estrous female, and record all
20 min continuous-time focal animal samples (Altmann, 1974) on all
occurrences of mating, mate guarding, agonism, and sexual
adult males (N = 10) and females (N = 10) starting shortly after sunrise
presentations involving the female in estrus. We considered
(approximately 0700 hr) and ending shortly before sunset (approxi-
male mate guarding as a male’s defence of the estrous female
mately 1700 hr) each day, totalling 177 hr of data collected. Each
(Clutton-Brock, 1989), as well as close proximity to and “shadow-
animal was individually known, and was identified via unique physical
ing” of the estrous female (Parga, 2010a). All occurrences sampling
for male scent marking displays (and aggressive responses by other
animals) in the group continued during female estrus. Ad lib data
TABLE 1 Male dominance hierarchy in each group and numerical
basis for their ranks
were collected on physical manifestations of reproductive state in
females by noting any changes in genital swelling or color (Jolly,
1966; Hrdy & Whitten, 1987). In this study, the mating season
Male
Group
Rank
Percentage of
agonistic wins
HA
A1
1
82%
Resident
NO
A1
2
73%
Resident
FK
A1
3
69%
Resident
AL
A1
4
47%
Resident
EC
A1
5
40%
Resident
All research protocols were approved by the School Ethics Committee
DV
A1
6
8%
Resident
and the University Ethics Board of Roehampton University
ED
C1
1
96%
Resident
(#LSC 17/215; Feb. 2010) and conform to the governing laws of the
HF
C1
2
67%
Resident
FE
C1
N/A
N/A
Immigrant
DF
C1
N/A
N/A
Immigrant
Residence status
commenced when the first female of the season was observed to
enter estrus. The weeks prior to the first observed estrus were
considered the non-mating season.
2.3 | Ethics statement
Malagasy Republic. This study was conducted with the approval of the
De Heaulme family, owner of the private nature reserve of Berenty.
This research adhered to the American Society of Primatologists
Principles for the Ethical Treatment of Non Human Primates.
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2.4 | Statistical analysis
The study period encompassed olfactory communication from males to
females both before and during estrus, as precopulatory female mate
choice could potentially occur during both periods. Hourly rates were
calculated for all male scent marking behavior, including for “anoint tail”
and “waft tail” to females only. Hourly rates were also calculated for male
mate guarding durations on days of estrus. To calculate female sexual
presentation rates, only those sexual presents given by estrous females
not being actively mate guarded were considered, because a male’s mate
guarding of a female can limit her proximity to other males, and
consequently, the number of sexual presents she directs to other males
(J.A. Parga and A. Walker-Bolton, personal observation).
To establish dominance rank for all resident males, focal data on all
decided agonistic interactions among males, including the direction of
submissive vocalizations known as the spat call (Jolly, 1966), were used
to generate dominance indices (Zumpe & Michael, 1986), from which
FIGURE 1
rank
Overall male scent marking rates by male dominance
ordinal dominance rankings were assigned to each male. Only analyses
involving dominance rank included resident group males. All other
appear to preferentially target high-ranked females for olfactory display;
analyses include resident and non-resident (immigrant) males.
a female’s dominance rank did not correlate with the rate of “anoint tail”
Aggression towards scent marking males was considered as that
and “waft tail” displays she received (rS = −0.074, N = 10, p = 0.840).
which occurred in the first 60 s following the ending of a tail anointing
In addition, overall scent marking by males was far less costly
and/or wafting display by a male towards a pre-estrous or estrous
(approximately eight times less costly) with respect to aggression
female. Aggression included bite, chase, charge, and displacement of
received following the scent marking than was performing the “anoint
the signaling male (Pereira & Kappeler, 1997). “Anoint tail” and “waft
tail” and “waft tail” displays to females. The average number of
tail” displays were recorded and treated as separate events. “Anoint
aggressive events after general scent marking (Table 2) was 0.2,
tail” is often followed by “waft tail,” but not in every instance.
whereas the average number of aggressive events after anoint tail and
We used Kolmogorov–Smirnov tests to determine normality.
waft tail events to females was 1.6. Only 11.1% of general scent
Because the data were not normally distributed, non-parametric
marking events (25 of 225) were followed by aggression to the scent
statistics were used, including Spearman rank correlation tests and the
marking male by males or females (Binomial test: p = 0.0001); in
binomial test. We conducted all analyses in SPSS 24.0 for Windows.
contrast, over 58% (72 of 124) of “anoint tail” and “waft tail” displays to
Significance was set at p < 0.05, and al... Purchase answer to see full attachment