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Habitat loss and degradation represent a major threat to Nearctic-neotropical migratory birds in the tropics. Managed agroecosystems have the potential to mitigate some impacts of land conversion, however, we know little regarding the quality of expanding oil palm plantation habitat for migratory birds in the neotropics. In this study, we used sex and age ratios, body condition, fat deposition, and muscle mass to assess oil palm habitat quality for seven species of migratory songbirds. Specifically, we captured individuals in native forest fragments and oil palm plantations in the state of Tabasco, Mexico, during two winter seasons (2017–2018, 2018–2019), and compared differences in age and sex ratios, and condition indices between habitats. We found that, when differences occurred, most species exhibited indicators of better habitat quality in native forest (older males with higher body condition indices) when compared to oil palm. Our results suggest that age and sex ratios combined with measures of physiological condition can be used to assess habitat quality for Nearctic-neotropical migratory birds overwintering in modified landscapes. Importantly, determining a species’ territorial behavior is key when selecting a given indicator of habitat quality for each species, and in certain cases, more intensive approaches such as estimates of survival, territory size, and food availability may be needed. Our results suggest that management strategies that promote forest-like conditions in oil palm plantations will improve habitat quality for declining populations of Nearctic-neotropical migratory birds.
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Ecological Indicators 139 (2022) 108964
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Original Articles
Do oil palm plantations provide quality habitat for migratory birds? A case
study from Mexico
Samuel L. Oliveira
a
,
*
, David J. Flaspohler
a
, Jessie L. Knowlton
b
, Jared D. Wolfe
a
a
College of Forest Resources and Environmental Sciences, Michigan Technological University, Houghton, MI 49931, USA
b
Department of Biology, Wheaton College, Norton, MA 02766, USA
ARTICLE INFO
Keywords:
Habitat quality
Age ratio
Sex ratio
Body condition
Neotropical migratory birds
Oil palm
ABSTRACT
Habitat loss and degradation represent a major threat to Nearctic-neotropical migratory birds in the tropics.
Managed agroecosystems have the potential to mitigate some impacts of land conversion, however, we know
little regarding the quality of expanding oil palm plantation habitat for migratory birds in the neotropics. In this
study, we used sex and age ratios, body condition, fat deposition, and muscle mass to assess oil palm habitat
quality for seven species of migratory songbirds. Specically, we captured individuals in native forest fragments
and oil palm plantations in the state of Tabasco, Mexico, during two winter seasons (20172018, 20182019),
and compared differences in age and sex ratios, and condition indices between habitats. We found that, when
differences occurred, most species exhibited indicators of better habitat quality in native forest (older males with
higher body condition indices) when compared to oil palm. Our results suggest that age and sex ratios combined
with measures of physiological condition can be used to assess habitat quality for Nearctic-neotropical migratory
birds overwintering in modied landscapes. Importantly, determining a speciesterritorial behavior is key when
selecting a given indicator of habitat quality for each species, and in certain cases, more intensive approaches
such as estimates of survival, territory size, and food availability may be needed. Our results suggest that
management strategies that promote forest-like conditions in oil palm plantations will improve habitat quality
for declining populations of Nearctic-neotropical migratory birds.
1. Introduction
Migratory bird demography is inuenced by multiple and disparate
habitats, often distributed across hemispheres, challenging conservation
and management efforts (Greenberg and Marra, 2005). Populations of
many species of Nearctic-Neotropical migratory birds have declined in
recent decades (Robbins et al., 1989; Butcher and Niven, 2007), with
estimates suggesting a dramatic loss of 2.5 billion birds over the past 50
years (Rosenberg et al., 2019). According to Johnson (2007), habitat
loss and degradation represent the greatest threat to bird populations.
Still, other factors such as building and window collisions, outdoor do-
mestic cats, and reduced populations of arthropods contribute to wide-
spread declines (Klem, 1990; Erickson et al., 2005; Loss et al., 2012;
Tallamy and Shriver, 2021). Identifying causal factors responsible for
population declines among migratory species is often complicated given
that experiences in distinct habitats, spread across hemispheres, can
interact to dynamically affect an individual birds tness (Sherry and
Holmes, 1995; Norris and Marra, 2007).
Broadly, bird populations may be limited by one or more discrete and
identiable factors, such as Brown-headed Cowbird (Molothrus ater)
parasitism and jack pine (Pinus banksiana) mismanagement diminishing
populations of Kirtlands Warbler (Setophaga kirtlandii) (Walkinshaw,
1983). Conversely, tness of individual birds may be affected by carry-
over effects, or interacting events experienced during different phases of
the annual cycle. Carry-over effects have been best described in Amer-
ican Redstarts (Setophaga ruticilla) whereby subordinate individuals can
be excluded from high quality winter habitats by dominant individuals,
resulting in worse body condition, later departure dates, and lower
reproductive success months later on the breeding grounds (Marra et al.,
1998; Cooper et al., 2015). Irrespective of whether bird populations are
regulated by discrete limiting factors, carry-over effects, or a combina-
tion of both, winter habitat quality often plays a key role in promoting or
limiting population growth (Norris et al., 2004; Newton, 2007; Latta
et al., 2016). Such relationship should be expected, especially when
* Corresponding author.
E-mail addresses: soliveir@mtu.edu (S.L. Oliveira), djaspo@mtu.edu (D.J. Flaspohler), knowlton_jessie@wheatoncollege.edu (J.L. Knowlton), jdwolfe@mtu.edu
(J.D. Wolfe).
Contents lists available at ScienceDirect
Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind
https://doi.org/10.1016/j.ecolind.2022.108964
Received 30 January 2022; Received in revised form 24 April 2022; Accepted 10 May 2022
Ecological Indicators 139 (2022) 108964
2
considering that Nearctic-neotropical migratory birds can overwinter
from six to eight months in the tropics (Runge et al., 2015).
In the neotropics, deforestation and land conversion for pasture and
row crops have been widespread for the last two centuries, with higher
rates since the middle of the twentieth century (Aide et al., 2013;
Graesser et al., 2015). Continued loss of winter habitat to agricultural
expansion may prevent population level recovery of several migratory
species (Faaborg, 2002; Rosenberg et al., 2016), like Wood Thrush
(Hylocichla mustelina), Golden-winged Warbler (Vermivora chrysoptera)
and Canada Warbler (Cardellina canadensis) whose population declines
have been linked to land conversion and deforestation in Central and
northern South America (Taylor and Stutchbury, 2016; Kramer et al.,
2018; Wilson et al., 2018). However, certain agroecosystems, such as
coffee plantations, can be managed to provide overwintering habitat for
some species (Tejeda-Cruz and Sutherland, 2004; Bakermans et al.,
2009), resulting in the creation of bird-friendly coffee certications that
promote specic management guidelines to enhance bird habitat.
Measures vary depending on the certication, but in all standards,
canopy height and cover as well as structural and oristic complexity are
part of the guidance to increase habitat quality (Gonz´
alez-Prieto, 2018).
Due to their economic importance, coffee and cacao have received the
majority of attention from researchers seeking to understand the value
of tropical agroecosystems for migratory birds. Additionally, the tradi-
tional or rustic coffee system used in warmer and drier environments,
known as shade-grown, can host similar communities of migratory birds
as those found in the native forest (Greenberg et al., 2000; Reitsma et al.,
2001; Gordon et al., 2007; Van Bael et al., 2007; Bakermans et al., 2009;
Bakermans et al., 2012; Philpott and Bichier, 2012; Colorado et al.,
2018; Gonz´
alez et al., 2020). Shade-grown plantations are characterized
by multistoried vegetation that mimics the structural complexity of
natural forest.
One of the most rapidly expanding crops in the global tropics is oil
palm (Elaies guineensis), which is grown for food and cosmetics (Foster
et al., 2011). Palm oil is the most widely used cooking oil on earth, with
global annual production rising from two million tons in 1970 to 71
million tons in 2018 (FAOSTAT, 2021). Overall, the majority of research
focused on the impacts of oil palm agriculture on biodiversity has been
conducted in Southeast Asia, where most of the global production is
located, and presented a considerable negative impact on the bird
richness and abundance following the conversion from native forest
(Donald, 2004; Aratrakorn et al., 2006; Edwards et al., 2010; Azhar
et al., 2011; Savilaakso et al., 2014). Bird richness and foraging guild
diversity also vary depending on farming systems, whereby smallhold-
ings - especially those practicing polyculture - exhibit better indicators
of habitat quality than plantation estates (Azhar et al., 2011; Azhar
et al., 2013; Azhar et al., 2014). Additionally, bird diversity was shown
to be lower in oil palm when compared to other agricultural habitats like
shaded cacao, rubber, and pasture (Donald, 2004; Fitzherbert et al.,
2008; Foster et al., 2011; Lees et al., 2015).
In Mesoamerica, Nearctic-neotropical migratory birds were shown to
be abundant in oil palm plantations in Southeast Mexico during the
northern hemisphere winter (Bennett et al., 2018; Moo-Culebro, 2018),
making this group of interest when investigating variation in over-
wintering habitat quality. Oil palm trees in this region are typically
grown on previously deforested areas formerly used as pasture for cattle
farming, in plantations with varying amounts of ground, understory, and
epiphytic plants permitted to share the plantation, which likely facilitate
the use of these plantations by some migratory birds (Bennett et al.,
2018; Oliveira et al., 2021). To date, only a few studies in Latin America
have assessed the value of oil palm plantations for migratory birds by
comparing patterns of richness and demographic measures of habitat
quality, such as overall and species-specic density in oil palm planta-
tion, native forest, and other agricultural systems (N´
ajera and Simonetti,
2010; Bennet, 2018; Moo-Culebro, 2018; Oliveira et al., 2021). Results
from these studies suggest that compared with pasture and other agri-
cultural crops, oil palm plantations contain a relatively rich diversity of
migratory birds. Still, the important question of whether oil palm
plantations serve as demographic sources or sinks remains poorly
understood.
Ornithologists have developed a variety of approaches to measure
relative differences in habitat quality for birds. Broadly, these fall into
two categories: 1) let the birds reveal habitat quality themselves by
using indices of tness (demographic measures, physiological condition,
and others), and densities, or 2) directly measuring the habitat itself
(food resources, vegetation, etc.) (Johnson, 2007). Identifying an
appropriate measure of habitat quality depends on several factors,
including how variation in habitat quality affects bird attributes such as
weight gain and territorial behaviors, which can decouple patterns of
density from habitat quality (Fretwell and Lucas, 1969; Van Horne,
1983; Johnson, 2007). Although not comprehensively studied, many
species of sexually dimorphic migratory birds display behaviorally
mediated habitat segregation on the wintering grounds, with older
males often occupying higher quality habitats compared to females and
younger males, a characteristic of the ideal despotic distribution model
(Fretwell and Lucas, 1969; Lynch et al., 1985; Ornat and Greenberg,
1990; Marra et al., 1993; Wunderle, 1995; Marra and Holmes, 2001).
For such species, assessing habitat quality by comparing density can be
misleading since high quality habitats are often occupied and defended
by dominant individuals, which exclude conspecics, meaning that high
quality habitats may, in theory, have lower densities. Thus, among
territorial migratory species, using age and sex classications may serve
as a meaningful index of hierarchical structures across a gradient of
habitat quality. Additionally, variation in body condition, fat deposition
and pectoral muscle mass across habitats may also provide valuable
insights into relative measures of habitat quality for migratory birds
(Holmes et al., 1989; Wunderle and Latta, 2000; Brown et al., 2002;
Johnson, 2007; Cooper et al., 2015).
Here, we assessed migratory bird habitat quality in oil palm plan-
tations and native forest using sex and age ratios and condition indices.
Given that native forest is characterized by higher structural and oristic
complexity relative to oil palm plantations (Oliveira et al., 2021), we
hypothesized that native forest would provide concordantly higher
habitat quality to migratory birds when compared to lower quality oil
palm plantations. Given our hypotheses, we predicted that we would
nd: 1) among territorial species, adult males will be over-represented
in higher quality native forest, while females and young males will be
over-represented in presumed poorer quality oil palm plantations; 2)
territorial species in higher quality native forest will show better phys-
iological condition than individuals inhabiting oil palm plantations; and
3) non-territorial species will exhibit equal age and sex ratios, as well as
equal physiological condition, across the native forest and oil palm
plantation habitats.
2. Methods
2.1. Study area
The state of Tabasco, in southeast Mexico, was covered by moist
lowland forest until the mid-1900s, when extensive deforestation and
the expansion of pasture and agriculture transformed much of the region
into a mosaic of second growth semi-deciduous forest, annual crops,
hardwood plantations, and pasture (Tudela, 1989; Salazar-Conde et al.,
2004; S´
anchez and Munguía, 2005; Arriaga-Weiss et al., 2008). Agri-
culture and livestock account for about 65% of the Tabascan territory,
including 20,000 ha of oil palm plantations (Briones-Salas et al., 2015;
SIAP, 2017). Government incentives fueled the expansion of oil palm
farming in the region about 25 years ago, primarily converting pasture
for cattle to oil palm plantations (Tudela, 1989). The average temper-
ature in the region is 24to 28 C, and precipitation ranges from 2,500 to
4,000 mm (INEGI, 2015). Most of our eldwork occurred during the cold
front season (NovemberFebruary). We conducted our samples in four
native forest patches (17.7478N, 92.7986W; 17.6495N,
S.L. Oliveira et al.
Ecological Indicators 139 (2022) 108964
3
92.8146W; 17.6198N, 92.8565W; 17.7936N, 92.850456W)
and seven oil palm plantations or estates (17.6133N, 92.8513W;
17.5788N, 92.8526W; 17.7667N, 92.7760W; 17.6473N,
92.8304W; 17.5714N, 92.8394W; 17.6992N, 92.9488W;
17.7652N, 92.7915W) in the municipalities of Jalapa, Tacotalpa and
Teapa (Fig. 1). All the forest patches were isolated, and not connected
with continuous primary forests which are conned to mountainous
areas. Native forest sites ranged from 11 to 276 ha (98.5 ±60.09 SE) and
oil palm plantations ranged from 15 to 84 ha (55.43 ±10.37 SE). Due to
logistical constraints, we focused our effort on similar ages of oil palm
plantations (~12 years) to control for variation in vegetation structure
due to oil palm growth. Plantations were managed similarly to the
smallholding farms in Southeast Asia, characterized by medium to small
sizes, independent owners, low use of mechanical harvest, and presence
of different age stands (Azhar et al., 2011; Azhar et al., 2014). Weed
management was done manually by workers using machetes, with no
herbicides used, differently than the common practices in Southeast Asia
(Tohiran et al., 2017). Additionally, no oil palm site sampled was
certied by the Roundtable on Sustainable Palm Oil (RSPO).
2.2. Field methods
We used 36 mm mist-nets (12 ×3 m) to capture migratory songbirds
in nine native forest plots and 21 oil palm plots within the aforemen-
tioned sites, with one to ten mist-nets opened in each of the plots. The
number of mist-nets opened was constrained by the number of trained
banders available and capture rates. Nets were opened shortly after
sunrise for four hours, except during rain. Fieldwork was conducted
during two winter seasons, the rst between 19 December 2017 and 27
March 2018, and the second between 16 October 2018 and 28 March
2019. The total sampling effort for the two seasons was 2,926 mist-net
hours, 1,140 h in native forest and 1,787 h in oil palm plantations. In
both seasons, we allocated more mist-netting hours to oil palm planta-
tions to increase our capture numbers in this relatively understudied
habitat. In the second season, we used playback to increase our capture
rate. The playback used was a 5 min owl-mobbing (developed by Ken-
neth Rosenberg and Ruth E. Bennet, Cornell Lab of Ornithology, 2015)
that proved to be effective in Guatemala (Bennett et al., 2018). It con-
tains the song of two owl species, Ferruginous Pygmy-Owl (Glaucidium
brasilianum) and Eastern Screech-Owl (Megascops asio), and alarm calls
from ten common migratory species. We broadcasted the recording for
15 min after opening mist-nets and repeated it each hour for another 15
min. On occasions when we caught high numbers of birds in the rst net
check, we did not repeat the owl broadcast to allow us to band and
process all the birds safely. All captured migratory birds were marked
with aluminum bands (United States Geological Survey), measured
(tarsus and tail length, wing chord, exposed culmen), weighed (±0.01
g), aged and sexed (following Pyle, 2007). We classied birds as either
adults, AHY (after hatch year) and ASY (after second year), or as young
HY (hatch year) and SY (second year). Fat deposition score was based on
a modied scale from Holmes et al. (1989), where we observed the
furcular fat and assigned a classication: N =no visible fat, L =13
strands of fat, S =strands of fat merging into a continuous sheet in some
places, H =fat nearly forming a continuous sheet but with some holes, F
=continuous sheet of fat lling the furcula and G =continuous sheet of
fat lling the furcula and spreading to other body parts. For pectoral
muscle classication we followed Tonra et al. (2013), where 0 =muscle
concave and keel prominent; 1 =muscle neither concave nor convex and
keel prominent; 2 =muscle slightly convex and keel still visible; 3 =
muscle convex and keel recessed.
2.3. Data analysis
2.3.1. Age and sex ratios
Previous research indicated that among territorial songbird species,
females and young males may be subordinate to older males and are
subsequently excluded from high-quality habitats (Marra, 2000). We
assessed species-specic social dominance by grouping young males and
Fig. 1. Location of the native forest and oil palm plantations where Neotropical migratory birds were captured in Tabasco, Mexico.
S.L. Oliveira et al.
Ecological Indicators 139 (2022) 108964
4
females, irrespective of age class, as subordinates to compare with the
adult male (dominant) group between habitats using a Chi-square test,
or Fishers exact test when at least one cell in the contingency table of
the expected frequencies was below ve (Bower, 2003). Segregation
patterns by dominants over subordinates are expected among species
that follow an ideal despotic distribution (Fretwell and Lucas, 1969).
However, for most overwintering migratory birds, it is unknown
whether this behavior exists, especially for non-dimorphic species (Al-
bert et al., 2020). Thus, we evaluated evidence for dominance hierar-
chies for species with enough captures, including those species in which
territorial behaviors on the wintering grounds is not yet known.
2.3.2. Condition indices
We generated a body condition index (mass corrected by body size),
where correlations between body size (wing chord) and body mass was
determined using a simple linear regression, where the residuals
represent variation in body condition (Marra and Holmes, 2001; Lab-
ocha and Hayes, 2012). We tested the residuals for normality and ho-
mogeneity of variance and then used a one-way ANOVA to determine
differences in body condition between forest and oil palm plantation. To
ensure we were using data only from the stationary wintering period,
excluding recent arrivals and birds preparing for spring migration, we
used Pearsons correlation analysis to test the relationship between day
of capture and body mass. Fat storage and muscle scores were analyzed
using the Wilcoxon rank sum test.
3. Results
Over two winter eld seasons we captured a total of 683 individuals,
242 in oil palm plantations representing 17 species of migratory birds,
and 441 individuals in native forest representing 21 species of migratory
birds (Table 1). Most of the sampled species did not have enough cap-
tures in both habitats to allow for statistical inference. Thus, we decided
to focus on species with at least nine individuals captured in both hab-
itats: American Redstart (Setophaga ruticilla), Hooded Warbler (Seto-
phaga citrina), Magnolia Warbler (Setophaga magnolia), Gray Catbird
(Dumetella carolinensis), Northern Waterthrush (Parkesia novebor-
acensis), Ovenbird (Seiurus aurocapilla), and Wood Thrush. Sex and age
class segregation were analyzed for those species with sexual dimor-
phism: American Redstart, Hooded Warbler, and Magnolia Warbler. For
non-dimorphic species, only age segregation was analyzed: Gray Cat-
bird, Northern Waterthrush, Ovenbird, and Wood Thrush. Other than
the Gray Catbird, all the assessed species are classied as insectivorous
during the winter (DeGraaf et al., 1985; Martin, 1985). From the seven
species assessed, ve of the species have exhibited population declines
in some part of their distribution, except for the Hooded Warbler and the
Northern Waterthrush (Sauer et al., 2017; Rosenberg et al., 2016; Dunn
and Hall, 2020; Smith et al., 2020). We were unable to assess habitat
quality of oil palm and native forest for resident birds due to few
captures.
American Redstart age and sex class distributions indicated a
dominance hierarchy where adult males were over-represented in native
forest (Fishers Exact Test, P =0.033, Fig. 2). Our analysis suggested that
the Hooded Warbler also exhibited a dominance hierarchy with adult
males found most frequently in native forest (Fishers Exact Test, P =
0.029, Fig. 2). Conversely, Magnolia Warbler did not show a signicant
difference in sex or age class distribution between habitats (Chi-squared
test, P =1, Fig. 3). We were only able to assess age distribution in non-
dimorphic species; for the Gray Catbird, there was no detectable
dominance hierarchy by age class (Chi-squared test, P =0.809, Fig. 4).
Northern Waterthrush also did not show age segregation (Chi-squared
test, P =1, Fig. 4). Ovenbird and Wood Thrush distribution did tend to
exhibit a higher proportion of adults in native forest (Fig. 5), although
we found no signicant difference between habitats (Fishers Exact Test,
P =0.378 and P =0.324, respectively). Both Ovenbird and Wood
Thrush may exhibit age or class segregation, but the small number of
individuals captured in oil palm plantations and the impossibility to
determine the sex in the eld could mask this pattern.
3.1. Body condition index
Three species differed in body condition between habitats (Table 2.
Fig. 6). American Redstart (ANOVA, F
(1,56)
=8.455, P =0.005) and Gray
Catbird (ANOVA, F
(1,101)
=4.883, P =0.029) showed higher body
condition in native forest. In contrast, Magnolia Warbler had signi-
cantly higher body condition in the oil palm plantations (ANOVA, F
(1,46)
=4.222, P =0.046). Wood Thrush body condition tended to be higher in
native forest, but the difference was not statistically signicant (ANOVA,
F
(1,59)
=1.1, P =0.299). The small sample size for Wood Thrush in the
oil palm plantation likely contributed to high variation, hindering a
more accurate assessment of Wood Thrush.
3.2. Fat storage and pectoral muscle scores
Two species differed signicantly with regards to the amount of
deposited fat between habitats, the Gray Catbird was the only species
that showed higher fat storage in the native forest (Wilcoxon rank sum
test, W =1131.3, P =0.037, Fig. 7); and, contrary to our prediction,
American Redstart had higher fat deposits in oil palm plantations
(Wilcoxon rank sum test, W =147, P =0.049). Our analysis found no
species with signicantly higher pectoral muscle scores in native forest
(Fig. 8). Conversely, Magnolia Warbler showed higher muscle scores in
oil palm plantations (Wilcoxon rank sum test, W =181, P =0.029).
4. Discussion
Habitat quality in the neotropics has been linked to demographic
changes in migratory bird populations (Albert et al., 2020). Expanding
oil palm agriculture in the neotropics, together with a high rate of
deforestation and land conversion threatens migratory bird populations.
While most researchers use audiovisual methods and estimates of den-
sity to assess habitat quality in the neotropics, we successfully used age
and sex ratios coupled with condition indices to assess relative differ-
ences in migratory bird habitat quality between native forest and oil
palm plantations.
Due to more complex vegetative structure in native forest when
Table 1
Neotropical migratory birds captured in native forest and oil palm plantation in
Tabasco, Mexico.
Species Native forest Oil palm
Cardellina pusilla 5
Catharus ustulatus 3
Dumetella carolinensis 91 20
Empidonax aviventris 5 1
Geothlypis formosa 32
Geothlypis trichas 4 28
Helmitheros vermivorum 29 1
Hylocichla mustelina 52 10
Icteria virens 17 2
Limnothlypis swainsonii 12
Mniotilta varia 7 1
Myiarchus crinitus 1
Parkesia noveboracensis 31 50
Passerina cyanea 1 11
Piranga rubra 1
Seiurus aurocapilla 40 9
Setophaga americana 1 2
Setophaga citrina 65 15
Setophaga dominica 2
Setophaga magnolia 28 23
Setophaga petechia 17
Setophaga ruticilla 9 49
Vermivora cyanoptera 2
Vireo griceus 6
S.L. Oliveira et al.
Ecological Indicators 139 (2022) 108964
5
compared to oil palm (Oliveira et al., 2021, Fig. 9), we hypothesized that
each study species would exhibit indicators of higher quality (older birds
in better condition) in native forest. Although most species adhered to
our predictions, surprisingly, a few exhibited elevated physiological
condition in oil palm plantations compared to native forest or showed no
signicant difference between the two habitats. American Redstarts, as
expected, exhibited a pattern consistent with adult male dominance in
native forest patches. The same pattern was found when comparing
populations in mangrove and shrub habitats in Jamaica (Marra et al.,
1993; Marra et al., 1998; Marra, 2000; Studds and Marra, 2008; Peele
et al., 2015), forest and shrub habitats in southern Mexico (Ornat and
Greenberg, 1990), and in primary forest in Venezuela (Bakermans et al.,
2009). Dominant adult males exclude young males and females of any
age class from high quality habitat, forcing them into suboptimal hab-
itats (Newton, 2008). In such situations, subordinate individuals may
adopt transient behavior, where individuals defend no territories and
exhibit longer distance movements compared with territorial birds
(Brown and Long, 2007). In the Dominican Republic and Jamaica, fe-
males and young males comprised most of the transient individuals of
American Redstart (Wunderle and Latta, 2000; Peele et al., 2015).
Overall, male-biased habitats are forested sites with wetter understories
(Sherry et al., 2020), likely reecting more stable invertebrate food re-
sources. Our results also suggested better body condition in American
Redstarts using native forest than in oil palm plantation. Such
Fig. 2. Age and sex class distributions of American Redstart (Setophaga ruticilla) and Hooded Warbler (Setophaga citrina) in native forest and oil palm plantation in
Tabasco, Mexico. Dominant =adult males. Subordinate =adult and young females and young males.
Fig. 3. Age and sex class distributions of Magnolia Warbler (Setophaga
magnolia) in native forest and oil palm plantation in Tabasco, Mexico. Domi-
nant =adult males. Subordinate =adult and young females and young males.
Fig. 4. Age class distributions of Gray Catbird (Dumetella carolinensis) and Northern Waterthrush (Parkesia noveboracensis) in native forest and oil palm plantation in
Tabasco, Mexico.
S.L. Oliveira et al.
Ecological Indicators 139 (2022) 108964
6
differences in body condition may reect sex and age segregation, and
subsequent cascading effects of segregation on tness during the
nonbreeding season (Marra and Holberton, 1998; Marra and Holmes,
2001; Studds and Marra, 2005). Interestingly, we documented redstarts
with higher fat loads in the oil palm when compared to native forest. In
some species, elevated fat stores may serve as insurance when faced with
unpredictable food resources in suboptimal habitat (Cooper et al.,
2015).
Likewise, Hooded Warbler showed adult male-biased segregation in
native forest patches. This result corroborates previous ndings where
males occupy mature forests and females are more commonly found in
shrub and disturbed habitats (Lynch et al., 1985; Morton et al., 1987;
Ornat and Greenberg, 1990; Stutchbury, 1994). Nevertheless, physio-
logical condition did not vary between forest and oil palm habitats.
Similarly, Conway et al. (1995) found no difference in Hooded Warbler
survival rates between mature and early successional habitats.
Furthermore, after experimental removal of territorial males from for-
ests, no females using adjacent shrub areas moved to the purportedly
higher quality vacant territories. This could indicate dissimilar habitat
selection across the sexes and/or non-exclusion by males. It may be that
Fig. 5. Age class distributions of Ovenbird (Seiurus aurocapilla) and Wood Thrush (Hylocichla mustelina) in native forest and oil palm plantation in Tabasco, Mexico.
Table 2
Means and standard errors of body condition indices from Neotropical migratory
birds captured in native forest and oil palm plantation in Tabasco, Mexico.
Species Native forest Oil palm
Setophaga ruticilla 0.233 ±0.11 0.043 ±0.04
Setophaga citrina 0.012 ±0.08 0.048 ±0.16
Setophaga magnolia 0.093 ±0.07 0.120 ±0.08
Dumetella carolinensis 0.268 ±0.28 1.112 ±0.51
Parkesia noveboracensis 0.151 ±0.13 0.092 ±0.13
Seiurus aurocapilla 0.017 ±0.18 0.077 ±0.3
Hylocichla mustelina 0.203 ±0.48 1.037 ±1.08
Fig. 6. Body condition index for Nearctic-Neotropical migratory birds in native forest and oil palm plantations in the state of Tabasco, southeast Mexico. Bars
represent standard error.
S.L. Oliveira et al.
Ecological Indicators 139 (2022) 108964
7
females are adapted to select secondary forest and shrub habitats during
the winter, reducing competition for territories and food resources with
males (Morton et al., 1987).
Our results suggested no dominance hierarchy among Magnolia
Warblers across native forest and oil palm at our study sites. Populations
of this species exhibited a tendency for females to select drier shrubby
habitats in Quintana Roo, Mexico (Ornat and Greenberg, 1990). Since
oil palm plantations have continuous canopy cover throughout the
winter, it is possible that changes in humidity are not as pronounced as
in the subdeciduous forests of the Yucatan Peninsula, resulting in similar
food resource distributions for Magnolia Warblers across habitats.
Additionally, among the Parulidae family, the Magnolia Warblers are
regarded as an adaptable bird, being found overwintering in a broad
range of habitats except recently cleared elds (Dunn and Hall, 2020); as
Fig. 7. Fat storage for Nearctic-Neotropical migratory birds in native forest and oil palm plantations in the state of Tabasco, southeast Mexico. Bars represent
standard error.
Fig. 8. Pectoral muscle scores for Nearctic-Neotropical migratory birds in native forest and oil palm plantations in the state of Tabasco, southeast Mexico. Bars
represent standard error.
S.L. Oliveira et al.
Ecological Indicators 139 (2022) 108964
8
such, this species likely does not exhibit a strong aversion to degraded
forest habitats (Reed, 1992; Robbins and Easterla, 1992). In fact, pop-
ulations in oil palm plantations had better body conditions and higher
pectoral muscle scores than those found in native forest. Food avail-
ability has been shown to drive Magnolia Warbler abundance (Johnson
and Sherry, 2001); thus, we hypothesize that Magnolia Warblers may
benet from less interspecic competition for food resources due to the
overall lower density of migratory birds in oil palm plantations (Oliveira
et al., 2021).
The Gray Catbird was the only non-sexually dimorphic species
assessed that exhibited dissimilar condition indices in native forests
when compared to oil palm plantations. Birds in native forest had better
body conditions and higher subcutaneous fat storage. Gray Catbirds tend
to select more forested sites during the winter compared to the breeding
grounds (Smith et al., 2020), likely due to habitat selection associated
with fruit availability (Martin, 1995). Gray Catbirds are known to have a
fruit-rich diet in the winter (Martin et al., 1961), and tree species rich-
ness is correlated with higher Gray Catbird density in native forest
patches (Oliveira et al., 2021). Fat deposition was also correlated with
habitat quality for Gray Catbirds during spring migration (Dunn, 2001),
showing that physiological condition may serve as a good indicator of
habitat quality for the species.
For Northern Waterthrush, no differences in age ratios or condition
indices were found between native forest patches and oil palm planta-
tions. Although this species has been shown to exhibit territorial medi-
ated dominance hierarchies on the wintering grounds (Smith et al.,
2010; 2011), we found no evidence of age segregation. Our results may
reect oil palm management at our study sites: high precipitation in the
wet part of the winter season is mitigated by digging channels crossing
the entire plantation to drain water and decrease ooding. Considering
that Northern Waterthrushes have preference for foraging on the ground
near wet soils, mud, water surfaces and pools (Smith et al., 2011; Rap-
pole and Warner, 1980), individuals may nd suitable habitats with
enough food during the winter months in these plantations (Smith et al.,
2010; 2011).
On the wintering grounds, Ovenbirds are known to prefer forested
sites, but can also use a variety of non-forested habitats (Rappole et al.,
1992; Porneluzi et al., 2020). The ability to pray on ants opportunisti-
cally, the main food item in the winter, may be related to their use of a
variety of habitats during the nonbreeding season (Strong, 2000), and
could explain their generalist behavior (Wunderle and Waide, 1993).
For example, in the Bahamas, Ovenbirds exhibited similar capture rates
and body mass in different habitats including shrub, mangrove, early
successional and secondary forest (Murphy et al., 2001). Sex and age
ratios were also similar among sedentary and oater individuals in Ja-
maica (Brown and Sherry, 2008). Our study was the rst to assess age
ratios and condition indices of Ovenbirds in oil palm plantations.
Similarly, we found no signicant differences in age ratios or condition
indices between habitats. Without the possibility of sexing individuals in
the eld, density and food availability seem to perform better as habitat
quality indicators for wintering Ovenbirds (Strong and Sherry, 2000;
Brown and Sherry, 2006; Oliveira et al., 2021).
Lastly, although Wood Thrushes tended to have higher body condi-
tion and an over representation of adults in native forest patches, we
failed to nd a signicant difference. The small sample size in oil palm
plantations (n =10) likely resulted in elevated variance and hindered
statistical inference. Also, wandering behavior is more common in poor
quality habitats (Winker, 1989), and this group can have higher fat
depositions than sedentary birds (Winker, 1990), which can complicate
the use of condition indices when territoriality cannot be determined.
McKinnon et al. (2015) monitored Wood Thrushes throughout the
winter and found faster declines in body condition, fat deposition, and
muscle mass among individuals using disturbed forest and shrubby areas
by the end of the season, when compared with mature forest. Addi-
tionally, females were more abundant in dry habitats in Belize and in
small fragments in Costa Rica, suggesting male mediated dominance
(Roberts, 2007; McKinnon et al., 2017). Considering that Wood Thrush
select forested habitats during the winter, territory densities may be
much lower in oil palm plantations than in native forest patches (Gra-
ham and Blake, 2001; Oliveira et al., 2021; Stanley et al., 2021), and
individual Wood Thrushes in oil palm may represent oaters occupying
a suboptimal habitat.
For species that did not exhibit a difference in age or sex class, or
physiological condition between native forest and oil palm plantations,
more intensive approaches such as mark-recapture for survival esti-
mates, territory mapping, or genetic markers for sex determination
should be used to assess habitat quality. For example, with knowledge of
sex, researchers found that Northern Waterthrushes increased and
decreased body condition in wet habitats and drier habitats, respec-
tively, when monitored through the entire winter; territoriality was
more common in wetter habitats and males showed more positive mass
changes than females (Smith et al., 2010; Smith et al., 2011). Ovenbird
body condition was positively related to food abundance during the
winter (Brown and Sherry, 2006). Similar to Northern Waterthrush,
Wood Thrush body condition declined throughout the winter in sub-
optimal habitats (McKinnon et al., 2015). Moreover, sedentary in-
dividuals had lower mortality rates than wanderers, which are more
commonly found in poor quality habitats (Winker et al., 1990).
Conversion of native tropical forest into oil palm has notable and
negative impact on avian diversity (Fitzherbert et al., 2008; Edwards
et al., 2010). Studies focused on the effect of oil palm plantations on
migrant birds in the Neotropics are scarce. As expected, our study sug-
gested that the native forest provides better habitat quality for most of
our study species. Nevertheless, some species can apparently adapt to
this recently introduced agroecosystem in the Americas, primarily
Fig. 9. Visualization of the Principal Component Analysis (PCA) ordination of
the difference in vegetation structure between oil palm plantations and native
forest fragments where we included tree height, understory density, tree den-
sity, tree richness, canopy cover, mean DBH (diameter at breast height), and
height of the tallest tree. Data were collected from six oil palm plantation sites
and ve native forest sites during the winter season of 20172018 in Tabasco,
Mexico. Ellipses represent 95% condence intervals around the centroid.
Reprinted from Migratory bird community structure in oil palm (Elaies gui-
neensis) plantations and native forest fragments in southern Mexico, by S. L.
Oliveira, D. J. Flaspohler, J. L. Knowlton, C. R. Webster and J. D. Wolfe, 2021,
Journal of Field Ornithology, 92.
S.L. Oliveira et al.
Ecological Indicators 139 (2022) 108964
9
generalists like Magnolia Warbler, Northern Waterthrush, Common
Yellowthroat, and Yellow Warbler (N´
ajera and Simonetti, 2010; Bennett
et al., 2018; Oliveira et al., 2021). Species that forage low in understory
and leaf litter for arthropods are considered vulnerable to deforestation
and habitat degradation (DeGraaf and Rappole, 1995), including loss of
structural complexity caused by oil palm cultivation (Oliveira et al.,
2021). Wood Thrush and Ovenbird are part of this group in our study
and tended to present better indicators in the native forest, although not
signicantly so.
According to Azhar et al. (2015; Azhar et al., 2017), the most widely
used oil palm certication (RSPO) does not account for important
managements that benet bird diversity, like habitat heterogeneity and
understory vegetative complexity. Studies conducted in shaded coffee
plantations highlighted the importance of structural and oristic
complexity (Gonz´
alez-Prieto, 2018), mostly based on birdsrichness and
abundance, and could be used as a baseline for the oil palm certication
in the Neotropics. However, it is recommended that requirements for
certications include further steps to increase the sustainability of oil
palm cultivation. A combination of demographic, distributional, and
individual indicators, accounting for each specieslife history, could be
adopted to assess the value of the oil palm agroecosystems for birds and
provide a tool to support certication programs for bird-friendly oil
palm.
4.1. Conclusion
Based on our ndings, we recommend several additional steps to
advance our understanding of anthropogenic habitat quality for
Nearctic-neotropical migratory birds in the tropics: 1) identify territorial
behaviors to determine if densities (for non-territorial species) or de-
mographics, age ratios, sex ratios, territory size should be used (for
territorial species); 2) sex and age segregation appears to be a useful
indicator of habitat quality for sexually dimorphic species where
dominant birds exclude individuals from good quality habitats; 3)
densities or direct measures of important resources (e.g., food abun-
dance) can be used for both territorial and non-territorial species.
Identifying why some working landscapes appear to provide higher
quality habitats relative to others represents an important line of inquiry
with potential to benets for declining populations of species that use oil
palm plantations such as Wood Thrush, American Redstart and Gray
Catbird (Rosenberg et al., 2016; Rushing et al., 2016; Smith et al., 2020).
Lastly, given that our results indicate that native forest provides higher
quality habitat than oil palm plantations, we should develop manage-
ment strategies that create forest-like conditions in oil palm plantations,
including increased oristic and structural complexity.
CRediT authorship contribution statement
Samuel L. Oliveira: Conceptualization, Methodology, Data cura-
tion, Investigation, Project administration, Writing original draft,
Writing review & editing. David J. Flaspohler: Conceptualization,
Funding acquisition, Methodology, Project administration, Resources,
Writing review & editing. Jessie L. Knowlton: Conceptualization,
Funding acquisition, Methodology, Writing review & editing. Jared D.
Wolfe: Methodology, Formal analysis, Writing review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing nancial
interests or personal relationships that could have appeared to inuence
the work reported in this paper.
Acknowledgements
We thank the eld technicians for their valuable work: Ruth A.
Regnet, Marco Antonio Torrez-P´
erez and Ingrid Tello-L´
opez. We also
thank the professors Ena E. M. Zayas, Stefan L. A. Weis, Cesar J. V.
Navarrete, Julio Cesar G. Castillo, and Lízbeth Y. Moo Culebro for
providing logistic support. We are grateful for the Wheaton College MA
and the College of Forest Resources and Environmental Science -
Ecosystem Science Center (ESC) for supporting travel and eldwork
commute, and the National Science Foundation - NSF and U.S. Depart-
ment of Agriculture for funding this study. Finally, we thank the editor
and the anonymous reviewers for their contributions for this
manuscript.
Funding
National Science Foundation Partnerships in International Research
and Education grant (grant number 1243444). USDA McIntire-Stennis
Cooperative Forestry Research Program.
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S.L. Oliveira et al.
... This species is considered a model for population dynamics studies in the tropics, including one of the earliest studies to demonstrate carry-over effects on migratory birds, showing that habitat quality in the winter can influence reproductive success in the summer ). Redstarts display territoriality and adult male dominance in the tropics, whereby adult males exclude females and young males from high-quality habitats like mangroves and primary and secondary forests , Oliveira et al. 2022. Subordinate groups are forced into suboptimal habitats , characteristic of the ideal despotic distribution model . ...
... This work is part of a project focused on the use of oil palm plantations by Nearcticneotropical migratory birds. Mist-netting was used to capture birds to assess habitat quality through various indicators, including species abundance, community composition, fitness indices, and age and sex segregation (Oliveira et al. , 2022. Concurrently with the bird captures (see Oliveira et al. 2022), we outfitted 16 American Redstarts with 0.3 g radio telemetry transmitters (Advanced Telemetry Systems model no. ...
... Mist-netting was used to capture birds to assess habitat quality through various indicators, including species abundance, community composition, fitness indices, and age and sex segregation (Oliveira et al. , 2022. Concurrently with the bird captures (see Oliveira et al. 2022), we outfitted 16 American Redstarts with 0.3 g radio telemetry transmitters (Advanced Telemetry Systems model no. 2414) attached using eyelash glue on the trimmed lower back of the birds. ...
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