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International Journal of Primatology (2022) 43:611
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635
Vol.:(0123456789)
https://doi.org/10.1007/s10764-022-00292-0
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Marking Versus Overmarking: Spatial andBehavioral
Patterns ofScent Marking inWild Diademed Sifaka
(Propithecus diadema)
LongondrazaMiaretsoa1· AndreaCascella1· LuigiVadàla1· DariaValente1,2·
ChiaraDeGregorio1· ValeriaTorti1· IvanNorscia1· JonahRatsimbazafy3·
OlivierFriard1· CristinaGiacoma1· MarcoGamba1
Received: 9 June 2021 / Accepted: 20 March 2022
© The Author(s) 2022, corrected publication 2022
Abstract
In mammals, olfactory communication plays an essential role in territorial and mat-
ing dynamics. Scent depositions in various species, including lemurs, can be placed via
marking or overmarking (marking over previous depositions). We focused on the role
that marking and overmarking play in territorial defence and intrasexual competition.
We investigated these aspects in diademed sifaka (Propithecus diadema) in the primary
rainforest of Maromizaha (eastern Madagascar). We collected scent marking data for five
groups from April to November 2018 and from May to December 2019. We aimed to
understand whether the lemurs deposited scent marks homogeneously across the home
range and whether sex, rank, and occurrence of intergroup encounters affected the lemur’s
deposition rate. We also asked whether males overmarked adult females more often than
other depositions, and the marking and overmarking rates changed between the migra-
tion and non-migration seasons. We found that scent marking was performed higher in
peripheral and overlapping areas than in the home range central areas. In addition, males
had higher scent marking rates, but intergroup encounters did not affect deposition rates.
Males showed higher rates of overmarking and primarily targeted dominant females’
depositions, particularly during the “migration” season (including premating and mating
seasons). Our findings suggest a border-marking strategy inPropithecus diadema. More
frequent scent marking in the “migration” season suggests intrasexual competition in
males. Our results suggest that marking is associated with territorial and resource defence,
suggesting that it plays a role in monopolizing females using a mate-guarding strategy and
may also serve for males’ self-advertisement to females and subordinate depositors.
Keywords Lemurs· Olfactory signals· Intraspecific communication· Territorial
defence· Ranging patterns
Handling Editor: Joanna Setchell
Cristina Giacoma and Marco Gamba Joint last authors.
Extended author information available on the last page of the article
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L.Miaretsoa et al.
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Introduction
Olfactory communication is an important part of social behavior for many mam-
malian species (Ralls, 1971; Enselberg and Kleiman, 1972). Scent marking (depo-
sition of scent signals from urine, faeces, or glandular secretions: Kleiman, 1966)
is a distinctive form of olfactory communication (Epple, 1986; Epple & Moulton,
1978; Schilling, 1979) aimed at conveying chemical signals to conspecifics (e.g.,
group members or neighboring conspecifics). An extensive body of studies shows
that scent marks are primarily status signals involved in territorial defence (Allen
etal., 1999; Braune etal., 2005; Brown & Macdonald, 1985; Coombes etal., 2018;
Gorman & Mills, 1984; Gosling & Roberts, 2001a, 2001b; Lewis, 2006) and intra-
sexual competition (Gosling & Roberts, 2001a; Muller and Manser, 2008; Kappeler,
1998; Lewis, 2005; Norcia etal., 2009).
In line with the territorial defence hypothesis, the scent marking rate increases on
days when intergroup encounters occur (Lledo-Ferrer etal., 2011; Roberts, 2012)
and the spatial distribution of scent marks maximizes the probability of detection
by an intruder (Gorman & Mills, 1984; Gosling, 1982; Gosling & Roberts, 2001b;
Lewis, 2006; Schilling, 1980). This hypothesis suggests that scent marking is related
to the size of the home range (Gorman & Mills, 1984). In species living in large
home ranges, territory owners may not be able to mark the entire perimeter and may
instead intensively mark the central part of the home range using the “hinterland”
marking strategy (Roper etal., 1993; Mills etal., 1980; Jordan etal., 2007; Begg
etal., 2003, 2005). In contrast, in species living in small home ranges, which are
economically defensible and where the boundary that must be patrolled is shorter
(Hamilton etal., 1976; Mitani & Rodman, 1979), overlapping and peripheral areas
may be intensively marked, as these are the areas with a higher probability of intru-
sion and where aggressive encounters occur (Brashares & Arcese, 1999; Lewis,
2006; Roberts, 2012; Rylands, 1990).Several studies of primates have reported that
the spatial distribution of scent marking supports a territorial defence function (Rob-
erts, 2012; Lewis, 2006; Mertl-Millhollen, 1979; Ryland, 1990). It was argued that
Saguinus fuscicollis used a “border marking strategy” by showing a higher scent
marking rate at the peripheral and shared area of their home range (Roberts, 2012).
Lemurs also scent marked areas close to the home range perimeter more than they
did in the core area (Propithecus verreauxi: Lewis, 2006) and deposited a higher
proportion of scent marks in overlapping areas than in the interior (Lemur catta,
and P.verreauxi: Merthl-Millhollen, 1986). These studies supported the territorial
defence hypothesis, which suggests that scent marks are essential to signal territorial
boundaries to conspecifics (Merthl-Millhollen, 1986; Lewis, 2006).
Because scent marking provides honest signals about the depositors’ quality
(Charpentier etal., 2008; Harris et al., 2018; Pochron etal., 2005b), the individ-
ual and temporal patterns of scent marking also can inform conspecifics about sig-
nal function (Lewis, 2006; Pochron etal., 2005a, 2005b). Because males often are
the sex with the highest intrasexual competition for access to mates (Kraus etal.,
1999) and mark at higher rates than females (Heymann, 2006; Pochron etal., 2005a;
Gould & Overdoff, 2002), scent marking also has been suggested to play a critical
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Marking Versus Overmarking: Spatial andBehavioral Patterns…
role in intrasexual competition (Kappeler, 1990, 1998; Lewis, 2005). In line with
this hypothesis, high-ranking males, who are highly engaged in reproduction and
intrasexual competition, scent mark at higher rates than subordinates to advertise
their status to conspecifics competitors (Lemur catta: Kappeler, 1998; Oda, 1999;
P. verrauxi: Kraus etal., 1999; Lewis & Van Schaik, 2007; Dall’Olio etal., 2012;
P. edwardsi: Pochron etal., 2005a, 2005b). Scent marking also increases at specific
times for the purpose of intrasexual competition. For example, a study of P. edwardsi
found an increased rate of scent marking during lactation and before the mating sea-
son when the dispersal of adult males occurs (Pochron etal., 2004, 2005b).
The rate of overmarking (placement of a scent mark directly on top of a previ-
ously deposited scent mark) increased before the mating season (Johnston et al.,
1994). The males of Hapalemur meridionalis overmarked female scent marks more
often when younger males were likely to disperse (Eppley etal., 2016). The authors
interpreted male lemurs immediately overmarking female depositions to conceal
females’ reproductive state to competitor males as a mate-guarding strategy (Eppley
etal., 2016; Kappeler, 1998; Lewis, 2005; Lewis & Van Schaik, 2007; Palagi &
Norscia, 2009).
Investigating lemurs for marking and overmarking is particularly interesting,
because they are smell-oriented primates and possess specialized scent glands
that show differences between males and females (Greene etal., 2019; delBarco-
Trillo etal., 2012; Charpentier et al., 2010; Elwell etal., 2021). Propithecus dia-
dema belongs to the family Indriidae and is one of the largest extant lemurs
(Mittermeier etal., 2010). It lives in mid-altitude, dense, humid rainforests in cen-
tral-eastern Madagascar (Powzyk & Mowry, 2003). It is a Critically Endangered
lemur that lives in multimale–multifemale groups (Irwin, 2020; Rasolonjatovo &
Irwin, 2020), occupies a home range of 21–83ha, and travels on average 837–987m
per day depending on habitat quality (Irwin, 2008). Each group comprises a domi-
nant adult male and a dominant adult female, with subordinate adults, subadults,
and juvenile individuals, where females dominate males (Rasolonjatovo and Irwin,
2019). We chose Propithecus diadema(Irwin, 2020), as a suitable species to inves-
tigate scent deposition patterns in their natural habitat. The species exhibits complex
scent marking behaviour by depositing scent odors from urine, faeces, and glandu-
lar secretions (sternal and anogenital glands) on different substrates (e.g., branches,
trunks), either in sequence or singularly.
We investigated the spatial and behavioural patterns of both marking and over-
marking in wild Propithecus diadema in the light of territorial defence and intrasexual
competition. We tested the following hypotheses. Assuming that Propithecus diadema
home ranges are economically defensible, we hypothesized that a long daily travel
path is helpful for the animals to patrol the whole perimeter, and we predict they will
increase the rate of scent marking (marking and overmarking) in peripheral and over-
lapping areas. Second, we hypothesized that if scent marking is linked to territorial
defence (Lledo-Ferrer etal., 2011; Roberts, 2012), we predict to observe an increased
scent marking rate (marking and overmarking) during the days of the intergroup
encounters. Third, we hypothesized that if male lemurs, including dominant males, are
subjected to intrasexual competition for mates, scent marking rate (marking and over-
marking) is highest in adult and dominant male depositors than in adult females and
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L.Miaretsoa et al.
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subordinates males. Fourth, as sifaka overmark females’ scent marks (intrasexual com-
petition by mate guarding), we predict males will immediately overmark females’ dep-
ositions to conceal females’ reproductive state against male competitors. Fifth, lemurs
increase vigilance during the migration period, where the bond formation of the repro-
ductive couple occurs. Thus, we predicted that Propithecus diadema increases the scent
marking rate (marking and overmarking) to deter migrating males.
Methods
Study Site andStudy Groups
We conducted field research in the Maromizaha New Protected Area in eastern Mada-
gascar, 6.5km from the junction to Andasibe (18° 56’ S, 48° 27’ E) and accessible
through the village of Anevoka. Maromizaha is a mid-altitude primary rainforest, cov-
ering 2,150ha and part of the Ankeniheny Zahamena corridor (Randrianarison etal.,
2015), harbouring 12 lemur species, including our study species. Group sizes range
from 4 to 11 in Maromizaha.
We studied five habituated groups of Propithecus diadema, focusing on patterns
of scent marking. The study lasted for more than 14months during two research
periods: April-November 2018 and May-December 2019. For a total of 108days
(870.50 ± 1.06h, mean = 8.03 ± 1.06h per day), we collected scent mark behav-
ioural data from 35 individuals: 21 males and 14 females (TableI). We consid-
ered three age classes. Individuals born during the study period were designated
as young, and animals older than 1year but less than 2years old at the beginning
of the data collection were considered subadults. The remaining individuals were
aged of 3.5years and above, in line with the species interbirth interval (1.5years:
Weir, 2014), they were assigned as adults. We assigned the season based on the
species reproductive schedule (Weir, 2014); Mating/Migration: November-Janu-
ary; Lactating/Migration: August-October; Birth: June-July; Gestation: February-
May. We observed mating attempts during late lactation (September–October: 2
cases) and early mating season (November: 1 case). In addition, we observed two
immigration/emigration cases during the study periods (1 case occurred in early
lactation season and 1 in mating season). Thus, we labelled events recorded dur-
ing the lactation/migration and mating/migration as part of the MIGRATION sea-
son; events occurring gestation and birth season, during which we observed no
immigration, were labelled as the NON-MIGRATION season.
Operational Definitions andBehavioral Data Collection
We defined “marking” as the act of depositing scent signals where no other scent
mark had been deposited the same day on the same spot by any group member
(Lewis, 2005). We defined “overmarking” when the mark overlapped a previous
scent mark by another group member entirely or partially (Johnston etal., 1994;
Jordan etal., 2010; Lewis, 2005; Pochron etal., 2005b). We used “scent mark”
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Marking Versus Overmarking: Spatial andBehavioral Patterns…
Table I Details of the Propithecus diadema study groups in the Maromizaha New Protected Area (April-November 2018 and May-December 2019). We include only indi-
viduals aged more than 6months. #Females that gave birth at least once during the study period; *Individuals born during the study; [+ 18] and [+ 19] respectively indicate
individuals that joined the group, and [− 18] and [− 19] those that left the group in 2018 and 2019. AD: adult; SA: subadult and Y: young; DOM: dominant, SUB: subordi-
nate; M: Male, F: Female, NA: not available as the individual was not yet present in the group
MARKING
(rate per hour) OVERMARKING
(rate per hour)
Nonmigration season Migration season Nonmigration season Migration season
Group Individual Sex Age Rank Days Mean SD Mean SD Mean SD Mean SD
2PD-MZ Kaly [− 18] M AD DOM 3 NA NA 1.800 1.740 NA NA 0.900 0.660
Gigi [+ 18] M AD DOM 21 0.007 0.360 1.860 1.140 0.360 0.300 0.720 0.300
Joby M AD SUB 25 0.300 0.180 0.420 0.480 0.180 0.060 0.240 0.180
Tsikivy M AD SUB 25 0.240 0.180 0.300 0.300 0.000 0.000 0.060 0.000
Blue M SA SUB 25 0.120 0.060 0.180 0.060 0.000 0.000 0.000 0.000
Tandra#F AD DOM 25 0.360 0.180 0.660 0.300 0.240 0.000 0.180 0.060
Onja#F AD SUB 25 0.300 0.180 0.540 0.420 0.060 0.000 0.120 0.000
Kintana F AD SUB 25 0.300 0.180 0.120 0.060 0.000 0.000 0.000 0.000
Voa F AD SUB 25 0.120 0.000 0.060 0.000 0.000 0.000 0.000 0.000
Green F SA SUB 25 0.180 0.060 0.180 0.060 0.000 0.000 0.000 0.000
3PD-MZ Fotsiloha [− 19] M AD DOM 15 0.660 0.360 1.140 0.840 0.480 0.300 0.600 0.360
Andry [+ 19] M AD DOM 7 NA NA 1.680 1.080 NA NA 1.140 0.540
Mike M AD SUB 24 0.360 0.240 0.720 0.780 0.000 0.000 0.420 0.360
Bisky M AD SUB 24 0.180 0.060 0.300 0.420 0.180 0.000 0.240 0.000
Pink M SA SUB 24 0.120 0.000 0.120 0.060 0.000 0.000 0.120 0.000
Orchide#F AD DOM 24 0.480 0.300 1.260 0.900 0.000 0.000 0.180 0.000
Siramamy#F AD SUB 24 0.180 0.120 0.300 0.120 0.000 0.000 0.180 0.060
Rahona [− 19] F AD SUB 15 0.240 0.120 0.060 0.000 0.000 0.000 0.000 0.000
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L.Miaretsoa et al.
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Table I (continued)
MARKING
(rate per hour) OVERMARKING
(rate per hour)
Nonmigration season Migration season Nonmigration season Migration season
Group Individual Sex Age Rank Days Mean SD Mean SD Mean SD Mean SD
4PD-MZ Feno M AD DOM 24 0.720 0.360 1.260 0.720 0.360 0.300 0.780 0.480
Tantely M AD SUB 24 0.600 0.540 0.600 0.540 0.180 0.060 0.240 0.120
Faly M AD SUB 24 0.300 0.180 0.420 0.420 0.120 0.000 0.180 0.060
Faniry M SA SUB 24 0.240 0.120 0.240 0.060 0.000 0.000 0.180 0.000
Volana#F AD DOM 24 0.780 0.420 1.320 0.840 0.120 0.000 0.120 0.060
6PD-MZ Hery M AD DOM 19 0.960 0.600 1.260 0.960 0.780 0.480 0.660 0.540
Hasina M SA SUB 19 0.180 0.180 0.540 0.420 0.180 0.000 0.000 0.000
Akondro* M Y SUB 6 0.120 0.000 0.120 0.000 0.000 0.000 0.000 0.000
Masina#F AD DOM 19 0.540 0.360 0.540 0.120 0.120 0.000 0.000 0.000
Diane#F AD SUB 19 0.480 0.360 0.780 0.480 0.000 0.000 0.120 0.000
Gavo* F Y SUB 6 0.120 0.000 0.120 0.000 0.000 0.000 0.000 0.000
8PD-MZ Tafita M AD DOM 16 0.780 0.540 1.620 1.560 0.240 0.180 0.420 0.300
Lova M AD SUB 16 0.420 0.240 0.480 0.000 0.120 0.000 0.000 0.000
Tia M AD SUB 16 0.180 0.060 0.660 0.780 0.000 0.000 0.000 0.000
Papay* M Y SUB 6 0.240 0.000 0.000 0.000 0.000 0.000 0.000 0.000
Afaka#F AD DOM 16 0.420 0.300 0.540 0.300 0.000 0.000 0.000 0.000
Litchi F SA SUB 10 0.180 0.000 0.000 0.000 0.120 0.000 0.000 0.000
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Marking Versus Overmarking: Spatial andBehavioral Patterns…
to indicate both marking and overmarking depositions (Lewis, 2005). We define
as an “event” any sequence of scent marking deposition, without interruption at
the same spot on a given substrate, through chest rubbing, anogenital rubbing,
and urine, or faecal deposition. We indicated as scent mark each single mark-
ing behaviour (e.g., anogenital rubbing, chest rubbing, and urination) in a scent
marking event. Thus, each marking “event” can be composed of one or multiple
marking “acts” (Heymann, 2000; Lledo-Ferrer etal., 2011).
We used all occurrences sampling (Altmann, 1974), collecting data
across all individuals in the group to maximize data collection on these
relatively infrequent behavioural events. We focused on one group for
3–4 consecutive days per week. On each sampling day, we reached the
group between 6:00 and 7:30 AM (before the start of the animals’ activ-
ity) and followed it until dusk (4:00 to 5:30 PM) when the animals went
to sleep.For each scent marking event, we recorded depositor identity,
the target substrate part (trunk or branch), and the time at which the
lemur deposited a scent mark. We also monitored whether another indi-
vidual followed, inspected, and scent marked on the same spot. Indeed,
after any scent mark event, two observers monitored the other individu-
als’ behaviour until the group members left the spot. We also recorded
the timing of the overmarking, whether it occurred within one minute,
within or after 5 min of scent deposition. Thus, we could identify the
overmarker (followers) and the first depositor.
Propithecus diadema use tree trunks and occupies the lower part of the
forest (Powzyk, 1997), allowing good visibility during scent marking deposi-
tion. We used natural marks, such as permanent scars and pelage variation,
to distinguish individuals. Two researchers and two research guides collected
data simultaneously, following different animals, to ensure that all group
members were visible at any time. If two or more observers witnessed a scent
marking deposition, we reached a consensus on the depositors’ identity and
the sequence of scent marking acts immediately after the observation. If an
observer had doubts about the depositor’s identity, he or she asked the others
to achieve consensus on identification. Four of five groups were small, with
4–6 individuals and 3–5 adults per group, and we could detect each group
member individually. The largest group (2PD-MZ) was more widely spread
than other groups (up to 40m). If we could not keep all group members in
sight, and if we did not observe adults, dominant, or reproductive individu-
als, we excluded this day from the behavioural and spatial analysis of scent
marking, but we still considered it for the group home-range estimation.
We also observed the behaviour of the group members during intergroup
encounters and on the following day to compare days with and without intergroup
encounters. If we could not observe the group on the following day, we used data
from the day before the encounter in our comparison instead (Lledo-Ferrer etal.,
2011). In addition to scent marking, we recorded aggressive interactions between
group members to determine the dominance hierarchy among individuals, using
all occurrences sampling (Altmann, 1974).
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L.Miaretsoa et al.
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Spatial Data Collection
We tracked and geo-referenced specific behaviors performed by the ani-
mals, including feeding, intergroup encounters, locomotion, and scent mark-
ing events (marking and overmarking), on a Garmin GPS MAP 78 S, with
precision ranging 3–10m. In addition, we recorded a new GPS point every
time the group members interrupted their activities and moved 20–50m away
from their previous location and engaged in the same or different behavior
(Bonadonna et al., 2017, 2020). When different behaviors occurred at one
GPS waypoint (from the same or different individuals), we coded the point
accordingly (example: feeding then marking). We recorded only one GPS
waypoint from if we observed several scent mark events at a single location
(e.g., deposited within a distance of less than 20m from the previous GPS
waypoint) by one or more individuals (e.g., in the case of overmarking). Our
points were not equally weighted since time spent at each location changed
according to the behaviors performed in each location.
Spatial Analysis
We analyzed spatial data in QGIS (QGIS development team, 2018) coupled with
ArcGis (ESRI, 2016). We performed all statistical analyses using R software (R Core
Team, 2018; version 3.6.1).
Home Range Size
We first estimated each group’s home range and identified overlapping areas
(the portion of the home range used by two or more adjacent groups) using
the Characteristic Hull Polygon method (95%CHP: Downs & Horner, 2009).
We used 95% CHP, because both the Minimum Convex Polygon (MCP) and
Kernel Density Estimation (KDE) tend to overestimate home range size
(Downs & Horner, 2009; MCP: Burgman & Fox, 2003; KDE: Walter etal.,
2011). Next, we calculated the home ranges with QGIS software (QGIS
development team, 2018) using spatial data collected during the 154days of
following (mean ± SD = 30 ± 4days per group; range: 23–35days), analyzing
2,281 GPS waypoints (mean ± SD = 456.20 ± 54.75 per group). We assessed
whether the number of days with spatial data collection was enough to com-
pute the groups’ home ranges by plotting the home range size against the
number of days of observation for each group. We extracted 10,000 random
combinations for each number of days and calculated the mean and standard
deviation of the Characteristic Hull Polygons (CHP).There is a slowdown
in the curve slope from left to right (group 3PD-MZ, 8PD-MZ, and 4PD-
MZ), indicating that the home range will not increase significantly even if
additional data are provided, except for 6PD-MZ and 2PD-MZ that seem still
climbing (Fig.1).
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Marking Versus Overmarking: Spatial andBehavioral Patterns…
Home Range Defendability
Home range defendability depends on an animal’s ability to monitor the perimeter
of its range to detect potential intruders (Hamilton etal., 1976; Mitani & Rodman,
1979). The defendability index (D) is defined as the ratio of observed daily path
length (d) to an area equal to the diameter (d’) of a circle with an area equivalent to
the home range area of the animal (D = d/d’). The term d’ is defined by the formula:
(4A/ℼ) ^0.5, whereArepresents the area of the home range of a given group; thus,
D = d/√ (4A/ℼ). When the index value is less than 1, the territory is considered not
defendable, whereas when the index value is equal to or higher than 1, the home
range is considered defendable (Mitani & Rodman, 1979). We applied this formula
to define the defendability index of each group’s home range. To do so, we first
measured each group’s daily travel path length (d) using ArcGIS software (ESRI,
2016), considering only days when we followed the group for the whole day (total of
136days), with a mean of 17 points per day (range: 7–32).
Use oftheHome Range
To assess the pattern of home range usage, we applied the gridding technique (Bona-
donna etal., 2020). First, we established a 0.216ha network of hexagons for each
home range using the data management tools in QGIS (QGIS development team,
2018). As we recorded a new GPS point every 20–50 m, the size of 0.216 ha is
Fig. 1 Accumulation curve computed by plotting the home range size (ha) against the number of days
of observations using the Characteristic Hull Polygon method for five groups of diademed sifaka (Pro-
pithecus diadema) in Maromizaha New Protected Area, Madagascar (April-November 2018 and May-
December 2019) (a-e). We computed the curve using 10,000 random combinations for each number of
days.
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L.Miaretsoa et al.
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appropriate to aggregate at least two waypoints per hexagon. Then, we aggregated
the hours spent by the group at each point location when engaging in a particular
behavior in each hexagon (Bonadonna etal., 2020) and the time between two suc-
cessive GPS points.
To define the central and peripheral area of the home range, we extracted the
centroid of each hexagon using the QGIS geoprocessing tool options. We defined
hexagons with a centroid more than 50m away from the home range boundary as
the “central area” and hexagons with a centroid less than 50m from the bound-
ary as “peripheral areas.” We focused on four groups that had at least one inter-
group encounter during data collection to identify the overlapping area. We defined
hexagons that were included at least in part in the shared area between two or more
adjacent groups as “overlapping areas.” We defined all the other hexagons as “nono-
verlapping areas.”
Spatial Distribution ofScent Marking
We pooled an individual’s scent marking (marking and overmarking events) per
GPS waypoint location. We then mapped the pooled geo-referenced scent marks
onto the groups’ home range. Next, we counted the marking and overmarking events
performed by each individual in each home range hexagon and for central, periph-
eral, overlapping and nonoverlapping areas using the QGIS analyst tool. We then
calculated the rate (events per hour) by dividing the scent marking count by the time
spent in each area. We calculated the timeframe by extracting the time that passed
between two successive GPS points.
To assess whether the scent marking changed depending on an individuals’ posi-
tion in the home range, we compared the rate of scent marking: 1) between the cen-
tral area and peripheral area (all 5 groups), and 2) between overlapping and nono-
verlapping areas (4 adjacent groups: 2PD-MZ, 4PD-MZ, 6PD-MZ, and 8PD-MZ).
Where the data were not normally distributed (Kolmogorov–Smirnov: P < 0.05) we
used a Wilcoxon matched-pairs signed-ranks test (hereafter, Wilcoxon test; Mundry
& Fischer, 1998; Siegel & Castellan, 1988). When data were normally distributed,
we used a paired t-test. We excluded one adult male from analysis because he left
the group (2PD-MZ) when we had sampled it for just 3days.
Analysis oftheBehavioral Data
First, we ran a steepness analysis to evaluate dominance hierarchy among individu-
als. We calculate the David’s Score for each lemur (i) by summing the proportion of
its wins during interactions with another individual divided by the number of inter-
actions with the other individual (w) with w2 (e.g., the summed w values of those
individuals with which i interacted). We then subtracted l, which represents the sum
of that particular individual’s losses against the other individual, and l2, which rep-
resents the summed l values of those individuals with whom i interacted (Shizuka &
McDonald, 2012). As females dominate males (Rasolonjatovo and Irwin, 2019), we
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Marking Versus Overmarking: Spatial andBehavioral Patterns…
analyzed males’ agonistic interactions (chase, bite, fight) separately from those of
females. We defined the individuals with the highest value of David’s score as domi-
nant and those with lower scores as subordinates (Shizuka & McDonald, 2012).
When intergroup encounter occurred, we quantified scent marking for each indi-
vdiual during the day of the intergroup encounter and calculated the rate by divid-
ing the total count by the individual observation time. We analyzed three groups,
namely 2PD-MZ, 6PD-MZ, and 8PD-MZ. We excluded an individual not sampled
during the intergroup encounters from the analysis. We also extracted the rate of
scent marking recorded on the following day (or the day before if data on the follow-
ing day were not available) and compared the rates. The data were not normally dis-
tributed (Kolmogorov–Smirnov,P < 0.05), and the sample size was limited, so we
used a Wilcoxon matched-pairs, signed-ranks test (Mundry & Fischer, 1998; Siegel
& Castellan, 1988) to compare scent marking rates on the day of encounter to those
on the day with no such encounter.
We then pooled the daily scent marking observations for each individual. Next,
we calculated the rate of marking and overmarking per hour by dividing the scent
marking counts by individuals’ daily observation time. Using these rates as the
response variables, we built Generalized Linear Mixed Effects Models (GLMMs)
using theglmmTMBpackage that can handle zero-inflated data (Brook etal., 2017)
in R studio (R Core Team, 2018; version 3.6.1) on data for all five study groups.
Our goal was to test whether the rate of occurrence is affected by sex, social rank, or
season considering only adults. We removed two adult males sampled on fewer than
8days or sampled for one season only from the analysis. We also excluded one adult
female, because including her values caused residuals to deviate from a normal dis-
tribution. We used theglmmTMBfunction to perform the model with the beta fam-
ily distribution. We built a full and a null model in which we set the scent marking
rates as the response variable (rate_min). We set the depositor’s sex (male, female),
rank (dominant, subordinate), and season (migration, nonmigration) as fixed fac-
tors and depositor identity (Nlevels = 23), group (Nlevels = 5), and day of sampling
(Nlevels = 108) as random factors. We also assessed the interaction between social
rank and season. We retained depositor sex, and the interaction between social rank
and season as fixed factors. We examined the variance inflation factors (VIF pack-
age; Fox & Weisberg, 2011) to exclude collinear predictors. We used an inclusion
threshold of VIF < 5, because VIF ≥ 5 may indicate considerable collinearity (Chat-
terjee & Simonoff, 2013; James etal., 2017).
We tested the full model’s significance (Forstmeier & Schielzeth, 2011) by com-
paring it against the null model, using a likelihood ratio test (ANOVA with argu-
ment test Chisq; Dobson, 2002). We used the R function “drop1” (Barr etal., 2013)
to calculate Pvalues for each predictor based on likelihood ratio tests between the
full and the null model. We checked whether the residuals were normally distributed
and homogeneous by looking at aqqplotcurve and the distribution of the residuals
plotted against the fitted values (DHARMa R package: Hartig, 2016).
Because we did not assess the interaction between sex and season, we ran a fur-
ther analysis to compare the marking rate for adult males and females across the
seasons (NONMIGRATION vs. MIGRATION). Because we could not fit a GLMM
model to assess the factors affecting the overmarking rate due to the limited number
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L.Miaretsoa et al.
1 3
of depositors (the model would not converge and the distribution of the residuals
highly deviated from a normal distribution), we also compared the male overmark-
ing rate targeting either male and female scent depositions between the NONMI-
GRATION and MIGRATION seasons. Because the data were not normally dis-
tributed (Kolmogorov–Smirnov, P < 0.05), we used Wilcoxon matched-pairs,
signed-rank tests for two paired samples (Mundry & Fischer, 1998; Siegel & Castel-
lan, 1988). We included only individuals that we observed for both periods in the
analysis. Finally, we used a Man-Whitney U test to compare the rate of overmarking
between sexes.
Ethical Note
We performed this study in the Maromizaha Protected Area, Central Eastern-Mad-
agascar, with research permits 91/18/MEF/SG/DGF/DSAP/SCB: 118/19/MEDD/
SG/DGEF/DSAP/DGRNE, 284/19/MEDD/SG/DGEF/DSAP/DGRNE and 338/19/
MEDD/SG/DGEF/DSAP/DGRNE, delivered by the Ministère de l’Environment et
du Development Durable (MEDD). During the study, we conducted only behavio-
ral observations without manipulating animals. All the information reported in this
paper result from our own data. The findings are not reported anywhere else. We
also declare that the data collection procedure conformed to the national legislation
and international regulation regarding animal welfare.
Results
Home Range oftheStudy Groups
The study groups occupied economically defensible home ranges with a mean size
of 20.7 ± 4ha (SD). Group 6PD-MZ had the largest home range (95% CHP: 25.5ha)
and shared 25.5% (6.5 ha) of its home range with at least three adjacent groups
(4PD-MZ, 8PD-MZ, and 2PD-MZ; Fig.2). Group 3PD-MZ had the smallest home
range (HRSMEAN ± SD: 16.6ha) and did not overlap with the other study groups.
Overall, the study groups traveled a mean daily travel path length of 720.1 ± 106m.
The home range defendability index (D)across all groups was 1.4 ± 0.2. Only 1 of
5 adjacent groups did not share part of its home range with any of the other study
groups.
The mean home range overlap between four adjacent groups was 13 ± 12%
(Fig.2b), and 10 intergroup encounters occurred in these overlapping areas. Each
group used an area of 17.7 ± 1.5ha exclusively.
Scent Marking Spatial Distribution Pattern
Overall, the rate of marking deposition was significantly higher in the periph-
eral area than the central area of the home range (Matched-Wilcoxon test: N = 25,
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Marking Versus Overmarking: Spatial andBehavioral Patterns…
V = 23, P < 0.001). In particular, dominant males deposited scent marks at
higher rates at the home range border (paired t-test: t (5) = − 3.097; Padj = 0.02
7) (Fig. 3a). In contrast, dominant females (N = 5; V = 0, Padj = 0.062; Fig. 3b),
subordinate males (N = 8, V = 7, Padj = 0.148), and subordinate females (N = 6,
V = 3, Padj = 0.156) did not show a significant preference for either peripheral or
central areas (Figs.3c-d).
Overall, males overmarked more in the peripheral than in the central zone of the
home range (matched Wilcoxon test: N = 14, V = 13, Padj = 0.025). In particular,
dominant males overmarked at a significantly lower rate in the central area (Fig.3e)
than the peripheral area (N = 6, V = 0,Padj = 0.031). This was not the case for sub-
ordinate individuals (Fig.3f), which did not differ significantly in the rate of over-
marking across all areas (N = 8, V = 13,Padj = 0.933).
Individuals also marked at a signficantly higher rate in the overlapping than in the
nonoverlapping area (matched Wilcoxon test: N = 18, V = 17.5, Padj = 0.003). We
observed a similar pattern for male (N = 10, V = 17,Padj = 0.048) and female depos-
itors (N = 8, V = 2.5, Padj = 0.035) (Figs.4a-b). In particular, dominant depositors
Fig. 2 Maps of home ranges (95% Characteristic Hull method) and home range overlaps of five adja-
cent groups of diademed sifaka (Propithecus diadema) in Maromizaha New Protected Area, Madagascar
(April-November 2018 and May-December 2019). (a) Peripheral areas are in different colors for each
study group and the central area is represented by empty hexagons. (b) Overlapping hexagons are in light
green and non-overlapping areas are in white. The irregular shapes in each home range are not part of the
home range.
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L.Miaretsoa et al.
1 3
of both sexes showed higher rates of marking in the overlapping area than the non-
overalappint areas (Fig.4c; N = 8, V = 1.5,Padj = 0. 0.025). In contrast, we did not
find a significant difference (Fig.4d) between these two areas for subordinate indi-
viduals (N = 10, V = 10, Padj = 0.084). There was no significant difference in the
overmarking rate between overlapping and nonoverlapping areas for adult males
(Wilcoxon test: N = 9; V = 6,Padj = 0.055; Fig.4e).
Effect ofIntergroup eEncounter onScent Marking Behaviour
We observed ten intergroup encounters, of which only one ended in an
aggressive confrontation, including chasing and biting, and nine consisted of
distant confrontation, including jumping between branches and vocal displays
Fig. 3 Rate of marking (a-d) and overmarking (e-f) between central and peripheral areas in five adjacent
groups of diademed sifaka (Propithecus diadema) at the Maromizaha New Protected Area, Madagascar
(April-November 2018 and May-December 2019). Plots show scent marking rates for dominant males
(a and e), dominant females (b), subordinate males (c and f), and subordinate females (d). *P ≤ 0.05.
Whiskers indicate 5th/95th percentiles, the horizontal line gives the median, the box the 25th/75th per-
centiles, and open circles outliers. DOM: dominant depositors; SUB: subordinate depositors; n.s.: non-
significant.
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Marking Versus Overmarking: Spatial andBehavioral Patterns…
as Zzuss and Zzuss-Tsk (Valente etal., 2022). Only adult individuals of both
sexes participated in the physical confrontation and scent marking deposi-
tion. Although individuals marked more frequently on intergroup encounter
days than on days without an intergroup encounter, this comparison was not
significant (matched Wilcoxon test: N = 14, V = 32,Padj = 0.217). Neither
dominant (N = 6, V = 3, Padj = 0.156) nor subordinate adults (N = 8, V = 9,
Padj = 0.250) increased their marking rate significantly on days with inter-
group encounters. Intergroup encounters did not affect the overmarking rate
(N = 14, V = 13, Padj = 0.523). However, resident adult males often over-
marked adult male intruders’ and resident females’ deposition (e.g., 3 of 4
Fig. 4 Rate of marking (a-d) and overmarking event occurrence (e) between the overlapping and nono-
verlapping areas in four adjacent groups of diademed sifaka (Propithecus diadema) at the Maromizaha
New Protected Area, Madagascar (April-November 2018 and May-December 2019). Presented are the
rate of scent marking event in adult males (a and e), adult females (b), in dominant (c), and subordinate
(d) individuals from both sexes, and the rate of overmarking in adult males (e). Significant results (with
P value < 0.05) are highlighted with single star (*), result with P-value = 0.05 is highlighted with single
full stop (.) and nonsignificant results (with P value > 0.05) are represented by n.s. Whiskers indicate
5th/95th percentiles; the horizontal line gives the median, and the box gives the 25th/75th percentiles,
and open circles denote outliers. DOM: dominant depositors; SUB: subordinate depositors.
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L.Miaretsoa et al.
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scent marks deposited by intruder males from group 2PD-MZ were over-
marked by adult male in the group 8PD-MZ).
Effects ofSex, Dominance Rank, andSeason onMarking andOvermarking
For marking, the full model significantly differed from the null model
(full vs. null: χ2 = 62.788, df = 4, Padj < 0.001; Table II). We found a signifi-
cant difference in marking rate between sexes with males marking more fre-
quently than females (Table II). The model also showed that marking was
influenced by the social rank of depositors with dominant individuals mark-
ing at significantly higher rates than subordinates (TableII). There was clear
seasonality in marking, which occurred more frequently in the MIGRA-
TION season than in the NONMIGRATION season (Table II). Unlike domi-
nant depositors, the marking of subordinates did not differ between seasons
(Pairwise Tukey-test: DOM.MIGRATION—DOM.NONMIGRATION, Esti-
mate = 0.585; SE = 0.097, Z = 6.004,P < 0.001; SUB.MIGRATION—SUB.
NONMIGRATION;Estimate = 0.113,SE = 0.118;Z = 0.965,Padj = 0.760).
Both males and females showed a seasonal pattern of marking. The mark-
ing rate was significantly higher during MIGRATION than NON-MIGRATION
season in both males (matched Wilcoxon test: N = 13, V = 0,Padj = 0.002) and
females (N = 10, V = 3,Padj = 0.042).
We found a significant difference between the sexes with males overmark-
ing more often than females (Mann–Whitney U test: NMale = 15, NFemale = 11;
W = 25, Padj = 0.003): 96% of overmarking events (N = 544) were performed
by males, whereas only in 4% (N = 25) were by females. Moreover, males pref-
erentially targeted female scent marks (TableIII). Overall, the vast majority of
females’ depositions were overmarked by dominant males (TableIII). Overmark-
ing of female scent marks by males typically happened very quickly, within the
first 60s after deposition (> 82% of cases) and rarely more than 5min after depo-
sition (< 3.5%; Fig.5). Adult male overmarking rates on adult female scent depo-
sitions also were higher in the MIGRATION than in the NONMIGRATION sea-
son (matched Wilcoxon test: N = 13, V = 7, Padj = 0.041).
Table II Influence of fixed factors on marking rate of Propithecus diadema at the Maromizaha New Pro-
tected Area, Madagascar (April-November 2018 and May-December 2019): results of a reduced model
including only significant interaction (full vs. null: χ2 = 62.788, df = 4, P adj < 0.001). na: Not shown as
has no meaningful interpretation
Estimate SE df Likelihood
ratio test P
Intercept -4.703 0.106 na na < 0.001
SexMALE 0.237 0.102 1 4.709 0.020
rankSUB -0.510 0.118 1 13.766 < 0.001
Season MIGRATION 0.585 0.097 1 13.766 < 0.001
rankSUB:seasonMIGRATION 0.471 0.125 1 13.766 < 0.001
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Marking Versus Overmarking: Spatial andBehavioral Patterns…
Discussion
Marking rates in Propithecus diadema differed significantly between the periph-
eral and central areas of the home range, and between the exclusive areas and areas
shared with neighbouring groups. These findings support our first prediction, that
scent marking targets the area with a higher probability of signal detection by
Table III Absolute frequency and percentage of scent marking being overmarked, overmarked by adult
and by dominant males across seasons for Propithecus diadema at the Maromizaha New Protected Area,
Madagascar (April-November 2018 and May-December 2019). The first line is a count and the second
line with bold text is a percentage (%) of scent markings being overmarked
Number (%) of overmarked scent marks
SM depositors Season # scent mark-
ing events Overall By male By dominant
male
Adult female NONMIGRATION 322 155 154 145 Count
(48.1) (99.4) (93.5) %
MIGRATION 528 317 314 274 Count
(60.0) (99.1) (86.4) %
Breeding female NONMIGRATION 292 151 150 141 Count
(51.7) (99.3) (93.4) %
MIGRATION 521 317 314 274 Count
(60.8) (99.1) (86.4) %
Dominant
female NONMIGRATION 204 113 113 107 Count
(55.4) (100.0) (94.7) %
MIGRATION 417 270 269 234 Count
(64.7) (99.6) (86.7) %
Adult male BOTH PERIODS 1863 80 61 37 Count
(4.3) (76.3) (46.3) %
Fig. 5 Percentage of overmarkings of female scent depositions happening within 60s (MIN-1), the first
5min (MIN-5), and after the first 5 min (> MIN-5) after scent deposition in NONMIGRATION and
MIGRATION seasons. (a) Adult female scent marks overmarked by adult males and (b) reproductive
female scent marks overmarked by dominant males.
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L.Miaretsoa et al.
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neighbouring groups like in the periphery or zones of overlap with neighbouring
groups. We also found that P. diadema occupied economically defensible home
ranges in Maromizaha. These findings are consistent with a border-marking strategy
(Gorman & Mills, 1984) and in line with studies reporting that Verreaux’s sifaka
(Propithecus verreauxi) scent marked the boundaries of their home range more fre-
quently than the core area (Mertl-Millhollen, 1979; Lewis, 2006). However, when
analysed by sex, we found that the differences in marking at the territory’s borders
or in the central area are significant only for males but not for females. This finding
agrees with observations suggesting that motivation may differ between individuals
(Lewis, 2006).
Females may scent marks to advertise their reproductive status to extra-group
males (Lewis, 2006) or claim ownership of feeding resources (Palagi & Norscia,
2009). Our data suggest that subordinate individuals make scent marks across the
home range to advertise their presence. Overall, our findings are consistent with the
territorial defence hypothesis (Lewis, 2005; Pochron etal., 2005a, 2005b). They also
agree with studies of saddleback tamarins (Saguinus fuscicollis) that exhibited a
clear border-marking strategy by intensely marking the home range’s peripheral and
overlapping areas (Roberts, 2012). Our results showed that overmarking rates also
differed significantly between the peripheral and central areas but not between areas
shared and not shared with neighboring groups. This difference suggests a different
role for marking and overmarking. This finding also is in line with previous studies
of lemurs suggesting that the spatial distribution of overmarkings indicate a male
tactic related to intrasexual competition (Lewis & Van Schaik, 2007; Norscia etal.,
2009). Because previous studies suggested that dominant males are more often mat-
ing successfully with dominant females (Kappeler & Schäffler, 2008; Norscia etal.,
2009), they may specifically target female depositions if placed at the home range
border to conceal female reproductive status from male competitors. Future studies
with a larger sample size are needed to test this hypothesis.
In contrast with our second hypothesis, we did not find evidence that scent mark-
ing rate increased on days on which intergroup encounters happened (Lledo-Fer-
rer etal., 2011), possibly because direct competition for resources is only partially
based on the olfactory signals or because differences in the daily occurrence of
marking did not reflect on the daily rate.
In support of our third hypothesis, we found a clear intersexual difference in the
amount of scent marking events, with males depositing markings and overmarkings
at higher rates than females. This is in line with previous findings. For example,
in Milne-Edwards’ sifaka (Propithecus edwardsi), males scent marked almost twice
as often as females (Pochron etal., 2005a, 2005b). Male Propithecus verreauxi
also scent marked significantly more often than females (Lewis, 2005). Such evi-
dence has been linked to the intrasexual competition hypothesis, in which the sex
that competes more strongly for mates, scent marks more often than the other sex
(Heymann, 2006). In line with our prediction, our study also provided evidence that
dominant individuals mark at higher rates than subordinate individuals, as observed
in several other primate species, and in lemurs in particular. For example, studies
of Propithecus verreauxi(Lewis, 2005), and Propithecus edwardsi(Pochron etal.,
2005a, 2005b) reported that either dominant males or females scent marked more
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Marking Versus Overmarking: Spatial andBehavioral Patterns…
often than subordinates. In Lemur catta, dominant individuals also showed a higher
rate of scent marking than subordinates (Kappeler, 1990, 1998). Other studies found
that dominant sifaka are highly involved in reproductive and intrasexual competition
(Lewis & van Schaik, 2007), because they sire the large majority (> 90%) of off-
spring (Kappeler & Schäffler, 2008). In our study, dominant males also overmarked
significantly more often than subordinates. Previous findings on the biological mar-
ket of mating in P. verreauxi found that dominant males who overmarked more were
more likely to succeed in mating with reproductive females (Norscia etal., 2009).
Dominant adult male P. verreauxi had a higher rate of chest marking and copulated
more frequently with reproductive females than clean chested (mostly subordinate)
males (Dall’Olio etal., 2012). In conclusion, our findings, like those of other stud-
ies, suggest an influence of sex and especially social rank on scent marking and
odor-mediated intrasexual competition in hierarchical lemur societies.
Supporting our fourth prediction, adult and dominant males also overmarked
adult and breeding female scent depositions more frequently, but not male deposi-
tions. This intersexual difference in performing and receiving overmarking aligns
with the intrasexual competition hypothesis. In Propithecus verreauxi, males imme-
diately overmarked female scent marks, and researchers interpreted this behavior as
a form of mate competition between males (Lewis & Van Schaik, 2007). In other
primate species, males actively overmark mostly female scent depositions, which
suggests a mate-guarding function (Lemur catta:Kappeler, 1998;Saguinus fusci-
collis:Lledo-Ferrer etal., 2010; southern bamboolemur,Hapalemurmeridionalis,
Eppley etal., 2016). In P. diadema male overmarking occurred mainly within the
first 60s of female scent deposition. This behavior may serve to claim ownership
of the female or to conceal the female’s odor from male competitors. Thus, by scent
marking, females may advertise themselves as avaliable for mating, whereas males’
scent marking and overmarking may allow males to assess the competitive abilities
of other males (Kappeler, 1990), playing a role in intrasexual competition.
Finally, marking and overmarking showed seasonal differences, in agreement
with the hypothesis that they may play a critical role in advertising intersexual
competition for mates. This difference supporting our fifth prediction by show-
ing that adult dominant males and females scent marked at significantly higher
rates in the MIGRATION season. Scent marking may serve different functions
in the two sexes (Lewis, 2006; Pochron etal., 2005b). For our focal species,
the fact that adult and dominant males showed the highest marking rate in the
migration period could serve to intimidate and deter migrating adult male com-
petitors (Pochron etal., 2005b). The increase in the rate of overmarking also is
in line with intrasexual competition for mates, because it may serve the defence
of reproductive females from migrating same-sex competitors. This interpreta-
tion does not exclude territorial defence as a function of scent marking because
additional markings deposited in the migration period (premating/mating season)
may prevent competitors from neighbouring groups and immigrants from using
the resources present in the home range and occupying the home range when suc-
cessful reproduction is at stake. Both sexes scent marked significantly more in the
migration season than in the non-migration season. Such an increase may be fur-
ther associated with other factors. For example, during late lactation and the early
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L.Miaretsoa et al.
1 3
mating season, females may need more energetic resources to secure reproduction
success. Consequently, females may invest more in defending feeding resources
by increasing the scent marking rate. In addition, the offspring are closer at wean-
ing and become more independent during the early mating season, so they may
found beneficial to scent mark more often to communicate their identity to con-
specifics (e.g., to receive provisioning from their mothers).
Conclusions
Both forms of scent marking (marking and overmarking) are deposited nonran-
domly in the home range and follow a distribution pattern that may optimize sig-
nal detection, possibly because depositions are a limited resource and energeti-
cally expensive (Gorman & Mills, 1984; Roberts & Lowen, 1997). Furthermore,
the intrasexual competition hypothesis may explain the functional convergence of
marking and overmarking in males. Overall, this study contributes to understand-
ing the possible functional divergence of scent marking between lemur males and
females and is evidence of the multifunctional complexity of olfactory signalling
in lemurs.
Acknowledgements This research was funded by the University of Torino, Department of Life Sciences
and Systems Biology. Our thanks also to the Ministère de l’Environnement et du Developpement Durable
(MEDD) of the Malagasy government for the issuance of the research permit related to our research. Special
thanks to the Group d’Etude et de Recherche sur les Primates (GERP) de Madagascar, the current manager
of the Maromizaha Protected Area, for all administrative and logistic assistance during the research period.
Our special thanks go to Flavia Petroni for helping our team during field data collection. We are grateful
for the research guides, who helped us during data collection. Without their assistance, we could not have
achieved this work. We thank all the local people of Anevoka and the surrounding villages for making avail-
able the cooks and guardians for us during our field activity. Finally, we address our warmth thanks to all the
local authorities for their collaborative administrative assistance during our data collection period in Mar-
omizaha. We are grateful to two anonymous reviewers, guest editor Prof. Ute Radespiel, and Editor Prof.
Joanna Setchell, for their comments and help in improving the previous version of our manuscript.
Author Contributions L.M, I.N, D.V., C.D.G., M.G., O.F., and V.T. designed the research protocol. L.M,
A.C, I.N., O.F., and M.G. developed the methodology and performed the analyses. L.M., A.C., C.D.G.,
L.V. performed the fieldwork. L.M, M.G., J.R., I.N., V.T., O.F., and C.G. contributed to developing the
methods, interpreting the results, and provided editorial advice. L.M., M.G., I.N., V.T, C.D.G., and C.G.
wrote the manuscript.
Funding Open access funding provided by Università degli Studi di Torino within the CRUI-CARE
Agreement. This research was supported by the University of Turin and grants from the Parco Natura
Viva- Garda Zoological Parks (Verona, Italy). L. M. received a scholarship granted by the Compagnia di
San Paolo that covered part of the fieldwork expenses.
Data Availability The data sets analyzed during this study are available from the corresponding author or
downloadable from https:// github. com/ sciab ola/ IJOP_ MIARE TSOA_ OCT21.
Declarations
Conflict of Interest The authors declare that they have no conflict of interest.
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Marking Versus Overmarking: Spatial andBehavioral Patterns…
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Authors and Aliations
LongondrazaMiaretsoa1· AndreaCascella1· LuigiVadàla1· DariaValente1,2·
ChiaraDeGregorio1· ValeriaTorti1· IvanNorscia1· JonahRatsimbazafy3·
OlivierFriard1· CristinaGiacoma1· MarcoGamba1
* Marco Gamba
marco.gamba@unito.it
1 Department ofLife Sciences andSystem Biology, University ofTurin, Via Accademia
Albertina 13, Turin, Italy
2 Equipe de Neuro-Ethologie Sensorielle (ENES), Centre de Recherche en Neurosciences de Lyon
(CRNL), CNRS, INSERM, University ofLyon / Saint-Étienne, Saint-Étienne, France
3 GERP (Groupe d’Etude Et de Recherche Sur Les Primates de Madagascar), Antananarivo,
Madagascar
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