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Urbanization, habitat extension and spatial pattern,

threaten a Costa Rican endemic bird

Pablo Muñoz

*, Adrián García-Rodríguez

& Luis Sandoval

1. Laboratorio de Ecología Urbana y Comunicación Animal, Escuela de Biología, Universidad de Costa Rica, San Pedro,

San José, Costa Rica, 11501-2060; pablomgl94@gmail.com, biosandoval@gmail.com

2. Departamento de Zoología, Instituto de Biología, UNAM, AP 70-153, Ciudad Universitaria, CP 04510, Ciudad de

México, México; garciar.adrian@gmail.com

* Correspondence

Received 07-V-2020. Corrected 29-X-2020. Accepted 11-XI-2020.

ABSTRACT. Introduction: Migration of people from rural environments to cities has accelerated urbanization

and modified the landscape as well as the ecological processes and communities in these areas. The Costa Rican

endemic Cabanis´s Ground-Sparrow (Melozone cabanisi) is a species of limited distribution restricted to the

“Gran Area Metropolitana”, which is the biggest urban settlement of the country. This area has experimented

and still experiment an ongoing fragmentation and loss of habitat used by this species (coffee plantations, shrubs,

and thickets). Objective: To determine the effects of urbanization on habitat abundance and spatial pattern for

the occurrence of Melozone cabanisi. Methods: We modeled the area of potentially suitable habitat for this spe-

cies in Costa Rica using occurrence and bioclimatic data. Then, we estimated the actual suitable habitat using

land cover type layers. Finally, we analyzed the connectivity among the actual suitable habitat patches using

single-patch and multi-patch approaches. Results: From the area of potentially suitable habitat estimated by the

bioclimatic model, 74 % were urban areas that are unsuitable for Melozone cabanisi. The largest suitable patches

within urban areas were coffee plantations; which also were crucial for maintaining connectivity between habitat

patches along the species’ range. Conclusions: To preserve and protect the Melozone cabanisi, these areas must

be taken into consideration by decision-makers in the present and future management plans. We recommend

avoiding change shrubs and thickets to urban cover to preserve the occurrence of Melozone cabanisi, and imple-

ment a program for the payment of environmental services to landholders, supported by the local governments,

to protect those habitats in urban contexts.

Key words: coffee plantations; habitat loss; habitat connectivity; keyplayer; landscape ecology; maxent;

Melozone cabaninisi.

Urban areas are expanding and currently

support more than 50 % of the world’s popula-

tion leading to the transformation of natural and

rural environments into urban centers (Mont-

gomery, 2008; Aronson, Handel, La Puma,

& Clemants, 2015). Urbanization alters the

composition of biological communities and the

ecological relationships among their species

(Marzluff, 2017). Urban gradients often lead to

gains and losses of non-native and native spe-

cies, respectively (Lindenmayer, Cunningham,

Donnelly, Nix, & Lindenmayer, 2002; Lewis et

al., 2015). While the relative number of these

gains and losses across the gradient varies by

location (Blair, 1996), diversity is always low-

est in the urban core (Marzluff, 2001). Invasive

Muñoz, P., García-Rodríguez, A., & Sandoval, L. (2021). Urbanization, habitat extension

and spatial pattern, threaten a Costa Rican endemic bird. Revista de Biología

Tropical, 69(1), 170-180. DOI 10.15517/rbt.v69i1.41742

ISSN Printed: 0034-7744 ISSN digital: 2215-2075

DOI 10.15517/rbt.v69i1.41742

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species tend to be less affected by urbanization

due to their capacity to adapt to and use the

new habitats created (Lindenmayer et al., 2002;

Lewis et al., 2015). In contrast, species that

decrease in abundance or disappear are usu-

ally those that inhabit on the natural vegetation

before urbanization (Marzluff, 2001).

Habitat fragmentation is a process that

turns large and continuous habitats into smaller

patches with a different pattern from the origi-

nal and separated by others habitat types (Fah-

rig, 2003). Habitat fragmentation and habitat

loss can be considered independent process

(Fahrig, 2003), but in urbanization context is

difficult to separate their effects, as both happen

simultaneously (Hadley & Betts, 2016). Habi-

tat fragmentation may increase endogamy by

restricting gene flow among populations (Tem-

pleton, Shaw, Routman, & Davis, 1990; Jump

& Peñuelas, 2006), limit dispersion (Hanski

& Ovaskainen, 2000), and disrupt conspecific

attraction (Fletcher, 2009). Therefore, increases

in the probability of extinction of native spe-

cies are expected in highly fragmented habitats

(Jump & Peñuelas, 2006; Fletcher et al., 2018).

We used as a model species the recently

recognized Costa Rican endemic Cabanis’s

Ground-Sparrow (Melozone cabanisi, Passer-

ellidae) because is one of the species that may

be most affected by urbanization, due to its

reduced distribution in Costa Rica (Sandoval,

Bitton, Doucet, & Mennill, 2014; Sandoval,

Epperly, Klicka, & Mennill, 2017). Because

of that reason is classified by the government

of Costa Rica, after an expert evaluation, as

Critically Endangered (SINAC, 2017), con-

trary to the wrong UICN classification of Least

Concern justified in a suspected population

increase associated with an increase on habitat

result of the degradation of natural habitats

(BirdLife International, 2019. This species

originally inhabited areas with a native scrub

community, thickets, and young secondary

growth, near riversides or in forest gaps of the

Central Valley and Turrialba Valley (Sandoval

et al., 2014). Nevertheless, after habitat altera-

tions caused by agricultural expansion in both

regions, this species adapted to live in coffee,

sugar cane, squash plantations, and non-native

shrubs and thickets (Stiles & Skutch 1989;

Sandoval et al., 2014). Currently these habi-

tats are urban or industrial areas that contrary

to UICN information (BirdLife International

2019), its habitats are decreasing and fragment-

ing (Sánchez, Criado, Sánchez, & Sandoval,

2009; Biamonte, Sandoval, Chacón, & Bar-

rantes, 2011). This because those habitats are

not protected by any law and the majority of

habitats (if not all) occur outside of protected

areas (Sandoval et al., 2019). However, beyond

this information, nothing is known about the

current distribution of this species and their

populations related to the available habitat and

land cover types within their range.

Considering these knowledge gaps regard-

ing the current distribution and habitat avail-

ability for this species, here we aim to (1)

create an ecological niche model (ENM) to

determine the area of potentially suitable habi-

tat (sites of major bioclimatic suitability) for

the Melozone cabanisi, (2) estimate the current

suitable habitat area, and (3) analyze connec-

tivity among the current suitable habitat patch-

es for the study species. We proposed these

three objectives in order to assess the effect of

habitat quantity, quality, and spatial pattern on

Melozone cabanisi occurrence.

MATERIALS AND METHODS

We developed an ecological niche model

(ENM) to predict the area of potentially suit-

able habitat of the Cabanis’s Ground-Sparrow

in Costa Rica using the Maximum Entro-

py Algorithm (MaxEnt). This is a presence-

background method that correlates incomplete

information from occurrences and bioclimatic

predictors to establish suitable areas for a

given species (Elith et al., 2011). MaxEnt

quantifies the statistical relations between the

predictor variables associated with occurrence

points (precipitation of the driest month and

isothermality) and the background of the study

area (Muscarella et al., 2014). Then we identi-

fied the actual suitable area near the urban

centers by comparing the potentially suitable

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areas with a land cover map, after a model

selection process.

Occurrence Data: We obtained the occur-

rence data for Cabanis’s Ground-Sparrow from

three different sources: personal observations,

observations from colleagues, and occurrenc-

es available from eBird (www.ebird.org) and

the Global Biodiversity Information Facility

(www.gbif.org). From these three sources, we

gathered all the data occurrences with available

coordinates from 1817 (oldest) to 2015. In total

we gathered 472 occurrences that were filtered

to 37 occurrences and then used to build the

models. The reduction to 37 occurrences was

expected because Cabanis’s Ground-Sparrow

is a species of limited distribution and also, we

reviewed the data set by projecting all the com-

piled records with available coordinates onto

a map, discarded spatial outliers derived from

erroneous coordinate assignation or species

misidentification and occurrences closer to 1

km from each other to avoid pseudoreplication.

By the time this species was not recognized

as a separate one from Prevost´s Ground-

Sparrow (Melozone biarcuata), we selected

the occurrences from Prevost´s that were from

Costa Rica which corresponded exclusively to

Cabanis´s Ground-Sparrow.

Bioclimatic Predictors: We used as

predictor variables the 19 bioclimatic layers

available at www.worldclim.org at a 1 km

resolution (Hijmans, Cameron, Parra, Jones,

& Jarvis, 2005). This standard set of variables

are interpolations derived from global weather

stations mostly for the period between 1950

and 2000 based on precipitation and tempera-

ture and represent annual trends, seasonality

and extreme of limiting environmental factors

(Hijmans et al., 2005). Since our objective was

to create a predictive model, rather than an

explanatory model (Araújo & Guisan, 2006),

we used the entire set of bioclimatic variables

to run the models. MaxEnt works under a

machine learning approach (Olden, Lawler, &

Poff, 2008), meaning that the algorithm itself

can discriminate and assign the contribution

of each predictor variable used to generate the

models (Elith et al., 2011). To mitigate overfit-

ting models to the occurrence points (Merow,

Smith, & Silander, 2013), we delimited the

calibration area of the models using only the

bioclimatic information within 25 km radius

around each occurrence point.

Model Parametrization and Evaluation:

We generated the models using the pack-

age “dismo” (Hijmans, Phillips, Leathwick, &

Elith, 2016) after a tuning process conducted

with the package “ENMeval” (Muscarella et

al., 2014), in R 3.3.1. For model calibration, we

generated 80 tuned candidate models by vary-

ing two parameters: feature classes (FC) and

regularization multiplier values (RM, Merow

et al., 2013). The FC corresponds to differ-

ent transformations of the predictor variables,

which allows different fits of the observed data

(Elith et al., 2011). The RM values limit model

complexity by penalizing each additional term

included in the models in order to prevent

overfitting (Radosavljevic & Anderson, 2014).

We set the RM values from 0.5 to 4.0 at

0.5 increments and used 10 FC combinations

(FC = “L”,”Q”,”H”, “P”,”T”, “LQ”, “LQHP”,

“LQH”, “LHP”, and “LQHPT”; where L = lin-

ear, Q = quadratic, H = hinge, P = product and T

= threshold). We set 10 000 background points

for the evaluation of the models and used the

block method for data partitioning which splits

the data into four bins based on the latitude and

longitude lines that creates subsets of equal

numbers of localities, both occurrences and

background points (Muscarella et al., 2014).

We partitioned data to have testing and train-

ing bins for building the models (Muscarella et

al., 2014). We chose the block method because

it was the method that separates the localities

most equally from all the partition methods

and this is advantageous because the amount of

data used for testing the model is similar to the

data used for training.

We used the mean omission rate and the

area under the response curve (AUC) as met-

rics to select the best-fitted model (Muscarella

et al., 2014). Then we projected the selected

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model (potentially suitable area) to the rest

of the country and superposed it with a land

cover type layer of Costa Rica’s Gran Área

Metropolitana (GAM) updated to 2005. This

land cover type layer despite being rather old,

reflected useful present day situation of habitat

availability, because by that time the major

changes in land use were already done (Morera,

Romero, & Sandoval, 2013). We consider that

the changes that may have happened between

2005 and 2020 are not significant to our pur-

poses which are to do a primary assessment of

Cabanis’s Ground-Sparrow with the available

data, prior to propose directed field research.

We did this to determine which areas, from

the potentially suitable area, correspond to the

actual suitable area. This layer was developed

by the Regional and Urban Planification Pro-

gram of the GAM, for the years 1986, 1996

and 2005, and spans 3.8 % of the total exten-

sion of Costa Rica with a classification based

on 17 different types of land cover (PRUGAM,

2005). Based on the existing knowledge of

the species’ natural history (Stiles & Skutch,

1989), we considered as remnants of habitat the

areas classified as shrubs, thickets, and planta-

tions (coffee, squash, cane sugar). For this, we

binarized the best-fitted model into suitable and

non-suitable areas using the minimum training

presence threshold, which assumes as suitable

all cells with probability values above the mini-

mum assigned to any of the points used to train

the model (0 % omission rate; Muscarella et al.,

2014; Radosavljevic & Anderson, 2014).

Connectivity Analyses of the Actual

Suitable Area: We used Patch Analyst exten-

sion for ArcGIS 10 to obtain descriptors of

different patches including: surface indices,

number of fragments, mean size of fragments,

standard deviation of mean fragment size, total

edge length, landscape edge density, and mean

edge per patch. These metrics were related

to all the patches in the matrix (Paudel &

Yuan, 2012). We used these metrics to analyze

the patch dynamics in terms of fragmenta-

tion, configuration, distribution, and edges of

habitat sites for Cabanis’s Ground-Sparrow.

We compared the changes through three time

periods using the GAM land cover type layers

for the years 1986, 1996 and 2005 (PRUGAM,

2005; Morera et al., 2013) to analyze if a ten-

dency exists in changes in the patch metrics

according to patch-type.

We decided to run both single and multi-

patch connectivity analyses because the former

considers the area of each patch, but focused

on each patch individually; while the latter con-

sider groups of patches as a whole, but do not

consider the area of the patches, and because

both are based on graph theory (Pereira, Saura,

& Jordán, 2017). We calculated the probability

of connectivity (dPC) for each patch in the

suitable habitat matrix for Cabanis’s Ground-

Sparrow based on a single-patch approach

using Conefor sensinode 2.6 (Saura & Torné,

2009). We focused on the dPC

conn

, which is one

of the three fractions that composed the dPC

index, because it indicates the patches that act

as important stepping stones between the other

patches and is also closer and more comparable

to pure centrality metrics as those implemented

in the “keyplayer” package (Pereira et al.,

2017). The dPC

conn

considers the topological

position of each patch in the matrix and the

area of the patches that they connect with, done

by removal experiments (Pereira et al., 2017).

We conducted a connectivity analysis

based on a multi-patch approach using the R

package “keyplayer” (An & Liu, 2016). For the

selection of the key sets of patches, we focused

on two of the eight centrality metrics imple-

mented in the package. We used fragmenta-

tion centrality and m-reach-closeness centrality

due to its ecologically applicable output sets

as proposed before (Pereira & Jordán, 2017;

Pereira et al., 2017). Fragmentation centrality

key sets are obtained by calculating the degree

of fragmentation (connectivity lost respect to

the overall connectivity) after the removal of a

patch or a group of patches from the network

(An & Liu, 2016; Pereira & Jordán, 2017). The

m-reach-closeness centrality metric measures

to what extent a patch or group of patches are

connected to the rest of the intact network (An

& Liu, 2016; Pereira & Jordán, 2017). For

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each centrality metric, we ran 10 iterations

to increase the chance of finding the global

optimum that is the best group of patches, of

a given size, among all possible combinations

in the patch matrix (Pereira & Jordán, 2017)

and chose the key set with the highest central-

ity score. These two analyses require the natal

dispersal distance of the study species as an

input to determine the connectivity among the

matrix, therefore we used a maximum natal

dispersal distance of 1 500 m reported for

the Rufous-Crowned Sparrow (Aimophila rufi-

ceps; Greenwood & Harvey, 1982). The closest

relative species (Sandoval et al., 2017), for

which natal dispersal information is available.

RESULTS

Model Parametrization and Evalua-

tion: We obtained 80 candidate ENM’s based

on different parameterizations to predict the

area of Cabanis’s Ground-Sparrow’ potentially

suitable habitat. The best-fitted model (mean

omission rate = 0.03; AUC = 0.70) was the one

using a regularization multiplier of 3.5 and a

threshold feature class (Fig. 1). We determined

that only 49 037.4 ha correspond to the actual

suitable habitat for Cabanis’s Ground-Sparrow

based on the occurrence of coffee plantations,

shrubs, and thickets (Fig. 2A).

Connectivity Analyses of the Actual

Suitable Area: A total of 1 206 (41 837.2 ha)

patches of coffee plantations and 717 (7 200.2

ha) patches of shrubs and thickets were ana-

lyzed. From those, the ten biggest patches for

each land cover category represented 74.3 and

36.3 % respectively. The biggest patches of

coffee plantations were located from Carrizal

to Sarchí in the province of Alajuela in the

Northwest side of the GAM, but the biggest

patches of shrubs and thickets are near San

Rafael of Escazú in San José province and

Paraíso in Cartago province towards the South

and Southeast of the area.

Fig. 1. Binarized projection of the best-fitted ecological niche model prediction out of 80 candidate models for the Melozone

cabanisi (Cabanis’s Ground-Sparrow) and georeferenced points along the GAM.

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The patch indices for the shrubs, thick-

ets, and coffee plantation (Table 1) indicated

that both surface areas (+16.16 %) and frag-

ment numbers (+17.7 %) increased from 1986

to 2005. However, the mean fragment size,

standard deviation, and the amount of edge

per patch decreased (1.30, 30.52, and 4.14 %

respectively). On the other hand, the amount of

edge relative to the landscape increased (11.35

%; Table 1). In summary, the area covered by

shrubs, thickets, and coffee fields increased in

general. Nevertheless, if the coffee plantations

are excluded, these indices show that the shrubs

and thickets decreased in size (from 1996 to

2005), and the bigger patches that existed in the

past suffered fragmentation producing a larger

amount of edge length per patch (EP, Table 1).

The 10 best patches for Cabanis’s Ground-

Sparrow that serve as steppingstones for the

overall connectivity according to the single-

patch analysis were located in the Northwest-

ern part of the matrix and four were amongst

the largest in all matrix (Fig. 2B). Nonetheless,

the best patch according to dPC

conn

(Fig. 2B)

was medium-sized and located at Center-North

of the matrix. The multi-patch analyses of the

Fig. 2. A. Actual suitable habitat patches of coffee plantations, shrubs, and thickets for Melozone cabanisi (Cabanis’s

Ground-Sparrow). B. Important steppingstone patches for Cabanis´s Ground-Sparrow connectivity according to the single-

patch analysis located towards the center of the matrix. Multi-patch analysis results; C. Corridor like set of suitable habitat

patches arrangement in terms of reachability, and D. Clustered set of suitable habitat patches in terms of fragmentation for

Cabanis’s Ground-Sparrow. E. Complementary suitable area patches selected by more than one analysis for the species.

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suitable habitat network showed that 10 most

important patches, in terms of reachability (Fig.

2C; KPr = 0.93), were more dispersed in the

network forming a corridor-like arrange. This

group of patches has different areas, ranging

from 7.2 ha to over 22 000 ha. Two of these

patches also coincided with the single-patch

results, the largest ones in the area. On the other

hand, the set of 10 most important patches

determined by fragmentation centrality (Fig.

2D; KPf = 0.85) were more grouped at the

center of the matrix near the periphery of urban

settlements of Northern Heredia and Alajuela

provinces and eastern San José province. In this

group, two of the patches were also selected as

the largest in the matrix by both single-patch

and multi-patch reachability analysis. Seven

of selected patches in fragmentation centrality

analysis were shared also in the results of the

reachability centrality analysis, corroborating

their importance to the overall patch matrix

connectivity (Fig. 2E).

DISCUSSION

Our model showed that the area of poten-

tially suitable habitat for Cabanis’s Ground-

Sparrow occured within the largest urban area

in Costa Rica. Historically, this region has

been the area with the highest urban and indus-

trial development in the country (Herrera et

al., 2014). The expansion has occurred from

city centers of San José, Alajuela, Heredia,

and Cartago provinces towards the periphery

forming a growth ring that reaches localities at

10 to 15 km from the urban center (PRUGAM,

2005). Currently, according to a study of Costa

Rica’s land cover type change (PRUGAM,

2005), coffee plantations, shrubs, and thickets

are the habitats that suffered a major decline in

the last 25 years, this was has been also docu-

mented in the change of the number of patches,

surface area, patch size (for coffee plantations),

and landscape edge density from 1996 to 2005

(Biamonte, Sandoval, Chacón, & Barrantes,

2011). Species with small distribution ranges

and low abundances, as the study species,

tend to be more threatened by the reduction

and fragmentation of the habitats inside urban

areas, than those with large distributions and

high abundances (Manne & Pimm, 2001).

Shrubs and thickets habitats where Cabanis’s

Ground-Sparrow occurred, are abundant dur-

ing the early urban development as we found

(Table 1), and are rarely included in manage-

ment plans (Sandoval et al., 2019). There-

fore, these habitats alongside the urban areas

will end eliminated or altered more quickly

(Askins, 2001), which is what happened from

1996 to 2005 (Table 1). These results support

the suggestions that the habitat for this species

is decreasing (Sánchez et al., 2009; Sandoval et

al., 2014) contrary to the information published

for UICN (BirdLife International, 2019).

TABLE 1

Patch analysis indices for the patches of suitable habitat inside the “Gran Área Metropolitana”

Index

Shrubs and thickets Coffee plantations Total

1986 1996 2005 1986 1996 2005 1986 1996 2005

S (ha) 3 882 24 516 8 993 43 494 48 331 46 042 47 377 72 847 55 035

P 743 2 668 922 1183 858 1 345 1 926 3 526 2267

PS (ha) 5 9 10 37 56 34 25 21 24

SDP (ha) 8 38 38 959 1 122 677 752 555 523

PP (m) 994 908 4 405 926 1 839 889 4 132 061 5 018 115 3 944 993 5 126 969 9 424 041 5 784 882

ED (m/ha) 4.7 20.6 8.6 19.3 23.5 18.5 24.0 44.1 27.1

EP (m/patch) 1 339 1 651 1 996 3 493 5 849 2 933 2 662 2 673 2 552

S = Surface area, P = Number of patches, PS = Mean patch size, SDP = Standard deviation of the mean patch size, PP =

Total edge perimeter, ED = Landscape edge density and EP = Mean edge per patch.

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According to the three complementary

patch analysis, the two patches that were cru-

cial for maintain the connectivity of Cabanis’s

Ground-Sparrow habitats were coffee planta-

tions at Northwestern portion of the urban

area. This highlighting the important role of

such type of land cover as stepping stones for

conservation of this ground-sparrow. The main

problem that may arise with the destruction

of these habitats is a significant loss of bio-

diversity. This area is heavily urbanized and

some of the few adequate areas for maintaining

biodiversity are coffee plantations, shrubs, and

thickets. Moreover, a decrease in the overall

connectivity within the natural habitat matrix

may occur, and this will affect the remnant

routes of passage for several other taxa (Per-

fecto, Rice, Greenberg, & Van der Voort, 1996;

Harvey et al., 2008). Even though the Cabanis´s

Ground-Sparrow can occur in either shaded or

not shaded coffee plantations, but the shaded

ones are always better for the overall mainte-

nance of biodiversity (Perfecto et al., 1996).

Their relative importance relies not on just in

the amount of surface area they cover but in

their particular location; the most important

coffee plantations occur in heavily deforested

areas, where are used as wintering grounds

for migratory birds or source of resources

in drought periods for resident species (Per-

fecto et al., 1996; Bakermans, Rodewald,

Vitz, & Rengifo, 2012; Biamonte et al., 2011;

Sandoval et al., 2019). Therefore, protect these

areas used by Cabanis´s Ground-Sparrow will

benefit also the migratory species and several

other resident species that use it.

The other patches could serve as second-

ary connectivity routes to maintain the indi-

viduals’ flow between patches. These patches

were considered secondary because they were

either part of both groups of patches from

the fragmentation and reachability analyses,

but not the largest in area, or the biggest

shrubs and thickets which are restricted to

the eastern (Paraíso, Cartago province) and

Southern (Escazú, San José province). These

patches connect the remnant habitat at East and

Southeast, with the biggest patches located at

Northwestern distribution. Although we were

conservative in using a distance of dispersal

of 1 500 m in the multi-patch analysis our

results showed the relative importance of these

patches for ground-sparrow movements. How-

ever, their higher levels of isolation, smaller

area compared to coffee plantations, and the

fact that they do not generate direct incomes

from economic activities, as coffee does, make

them more prone to disappear (Sandoval et

al., 2019). Moreover, most of the shrubs and

thickets were separated from the coffee planta-

tions by a complete urbanized area. Therefore,

we also suggest studying the dispersal ecology

of the Cabanis´s Ground-Sparrow, not only

to improve future connectivity analyses but

to delimitate with more accuracy the priority

areas for this species.

Our study points out the most impor-

tant patches of coffee plantations, shrubs, and

thickets inside the Cabanis’s Ground-Sparrow

distribution for its conservation. These findings

may be used to study and preserve other resi-

dent and migratory bird species that use those

patches such as warblers, flycatchers, orioles,

or tanagers (Perfecto et al., 1996), including the

threatened Golden-winged Warblers (Vermi-

vora chrysoptera) and Olive-sided Flycatcher

(Contopus cooperi). These habitat remnants

support not only the persistence and survival of

the endemic Cabanis’s Ground-Sparrows, but

are also a refuge for several other taxa that are

restricted to this type of habitats such as other

88 bird, 27 butterfly, and 10 mammal species in

Costa Rica (Sandoval et al., 2019).

Cabanis´s Ground-Sparrow is only one of

many species potentially threatened by urban-

ization and habitat loss in Costa Rica. This

also demonstrates that our knowledge about

endemic species and their population dynam-

ics in urban centers is still vague, especially

in the neotropics. However, this study shows

that initiatives about the conservation of this

species or any other can help to direct and pri-

oritize the areas of action, which is especially

crucial in the dynamic and chaotic environ-

ments that characterize urban centers. We hold

that it is strictly necessary to expand the view

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of conservation policies and include the impor-

tant role of coffee plantations, shrubs, and

thickets in the urban matrix for several taxa,

as demonstrated here with Cabanis’s Ground-

Sparrow. We propose to declare the detected

areas as conservation priorities due to their

vital importance for the species survival in this

urban context. Among the actions necessary

to guarantee the conservation of these areas

we suggest the following: avoid changing the

land cover type through the implementation

of pertinent land cover policies that mitigate

their fragmentation; implement a program,

supported by the local governments, for the

payment of environmental services or reducing

tax payments as an incentive to land owners,

apply for reforestation programs to enhance

connectivity among the rest of the matrix, and

foment the protection of areas in successional

states by their controlled management. We sug-

gest that UICN need to re-evaluate Cabanis’s

Ground-Sparrow classification based on this

information about habitat availability and frag-

mentation, and previous publications (Sánchez

et al., 2009; Biamonte et al., 2011; Sandoval

et al., 2014). Finally, our analyses on potential

species distribution, patches importance, and

connectivity between patches is a tool that

will help to detect which habitats within heav-

ily urbanized areas are the most important to

ensure different species conservation.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGEMENTS

We thank J. Pereira for her useful sugges-

tions and advice on building the distance matrix

used in the multi-patch analysis. We thank M.

Picon and J.P. Hidalgo for language help

provided in the last stages of the manuscript.

We also thank researchers, bird observers and

all the people that submit their observations to

online platforms and make them accessible.

This work was supported by grant number

B9-123 of Vicerrectoría de Investigación, Uni-

versidad de Costa Rica to LS; AGR was sup-

ported by DGAPA Postdoctoral Fellowship at

Instituto de Biología, UNAM.

RESUMEN

Urbanización, cantidad de hábitat y distribución

espacial, amenazan un ave endémica de Costa Rica.

Introducción: La migración desde ambientes rurales hacia

las ciudades ha incrementado la urbanización. Esto ha

modificado el paisaje, así como los procesos ecológicos y

comunidades dentro de estas áreas. El Cuatro-ojos de Jupa-

roja (Melozone cabanisi) es una especie distribuida princi-

palmente al interior del asentamiento urbano más grande

de Costa Rica. Hasta el presente esta área sigue experi-

mentando fragmentación y pérdida del hábitat utilizado por

esta especie (plantaciones de café, charrales y tacotales).

Objetivo: Determinar los efectos de la urbanización sobre

la cantidad de hábitat y su distribución espacial, basada en

datos de presencia para M. cabanisi. Métodos: Modela-

mos el hábitat potencialmente adecuado para M. cabanisi

utilizando datos bioclimáticos y de presencia. Luego esti-

mamos el hábitat real utilizando el hábitat potencialmente

adecuado y las capas de cobertura del suelo. Finalmente

analizamos la conectividad entre los parches de hábitat real

utilizando un enfoque multi y mono-parche. Resultados:

Del área del hábitat potencialmente adecuado estimada

por el modelo bioclimático, 74 % fueron áreas urbanas,

lo que consideramos es un porcentaje inadecuado para M.

cabanisi. Los parches más grandes de hábitat real dentro de

las áreas urbanas fueron plantaciones de café, que a su vez

fueron cruciales para mantener la conectividad entre los

parches a lo largo del rango de distribución de la especie.

Conclusiones: Para conservar y proteger a M. cabanisi,

los tomadores de decisiones deben tener en cuenta los

charrales, tacotales y cafetales dentro de la distribución de

las especies en los planes de gestión presentes y futuros,

evitando su cambio a coberturas urbanas.

Palabras clave: plantación de café; pérdida de hábitat;

conectividad de hábitat; keyplayer; eología del paisaje;

Maxent; Melozone cabanisi.

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