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Latitudinal pattern in plant composition along the


Peruvian and Chilean fog oases
a

R. Manrique , C. Ricotta , C. Ferrari & G. Pezzi


a

Department of Agricultural Sciences, University of Bologna, Via G. Fanin 50,


IT-40127Bologna, Italy
b

Department of Environmental Biology, University of Rome "La Sapienza", Piazzale Aldo


Moro 5, IT-00185Rome, Italy
c

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Department of Biological, Geological and Environmental Sciences, University of Bologna,


Via Irnerio 42, IT40126Bologna, Italy
Accepted author version posted online: 15 May 2014.Published online: 29 May 2014.

To cite this article: R. Manrique, C. Ricotta, C. Ferrari & G. Pezzi (2014) Latitudinal pattern in plant composition along the
Peruvian and Chilean fog oases, Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology: Official
Journal of the Societa Botanica Italiana, 148:5, 1002-1008, DOI: 10.1080/11263504.2014.918059
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Plant Biosystems, 2014


Vol. 148, No. 5, 10021008, http://dx.doi.org/10.1080/11263504.2014.918059

ORIGINAL ARTICLE

Latitudinal pattern in plant composition along the Peruvian and


Chilean fog oases
R. MANRIQUE1, C. RICOTTA2, C. FERRARI3, & G. PEZZI3
Department of Agricultural Sciences, University of Bologna, Via G. Fanin 50, IT-40127 Bologna, Italy; 2Department of
Environmental Biology, University of Rome "La Sapienza", Piazzale Aldo Moro 5, IT-00185 Rome, Italy and 3Department of
Biological, Geological and Environmental Sciences, University of Bologna, Via Irnerio 42, IT-40126 Bologna, Italy

Downloaded by [OARE Consortium] at 16:27 25 December 2014

Abstract
Fog oases in western South America (locally named lomas) are distributed in a kind of fragmented or patchy way into the
coastal desert. Their origin, as well as their current ecological connections in terms of species dispersal capability, remains
an open question. We analyzed the latitudinal pattern in plant species and phylogenetic similarities of 13 lomas, which cover
the latitudinal extent of these habitats, from 78580 to 268150 S. A data-set of 1004 species from available checklists was
considered. Plant species composition and phylogenetic relationships among lomas were analyzed by non-metric
multidimensional scaling. Our results show three main groups of lomas (northern Peruvian, southern Peruvian, and
North-Central Chilean lomas) that are aligned along a complex, nonlinear north south gradient in ordination space.
The weak species overlap between Peruvian and Chilean lomas, together with the higher content in endemic species of the
Chilean communities, supports the hypothesis that, at least recently, species composition of the three main groups of lomas
has been shaped by desert barriers limiting plant dispersal.

Keywords: Floristic composition, insular communities, lomas, nonmetric multidimensional scaling, phylogenetic distances

Introduction
Much of the western coast of South America from
northern Peru to northernmost Chile (, 58 308S
latitude) is occupied by the Peruvian and the
Atacama deserts, which form a continuous hyperarid
belt at the base of the Andean Cordillera broken only
by occasional river valleys. These hyperarid conditions are due, on the one hand, to the presence of
the Andes that isolate the coastal deserts from the
eastern weather patterns and, on the other hand, to
the stable temperatures resulting from the influence
of cool sea surface temperatures associated with the
flow of the Humboldt Current (Dillon et al. 2003).
This high temperature stability, combined with the
constant position of the subtropical anticyclone,
results in a mild, uniform coastal climate with the
regular formation of thick fog banks below 1000 m
during the winter months.
Where these fog banks are intercepted by isolated
mountains or steep coastal slopes, they give rise to

characteristic fog oases hosting unusually rich


plant communities termed lomas formations, meaning small mountains (Reiche 1938; Weberbauer
1945; Ferreyra 1953; Ellenberg 1959). Besides fog
banks, an important role in maintaining the floristic
diversity of lomas is played by recurrent El Nino
events that occasionally stimulate short periods of
heavy rainfall bringing wet tropical conditions within
the deserts (Dillon 1985; Dillon & Rundel 1990).
Over 100 lomas are distributed along the western
coast of Peruvian and Chilean deserts (Oka & Ogawa
1984; Dillon 1997; Munoz-Schick et al. 2001).
Lomas are important germoplasm reservoirs that
host many endemic species, mostly concentrated in
northern Chile (Dillon & Hoffmann 1997; Pinto &
Luebert 2009) and southern Peru (Galan de Mera
et al. 2011). About 847 plant species are known in
the Peruvian lomas (Dillon et al. 2003; Dillon et al.
2011), while 433 species are known in the Chilean
areas (Larran 2007). Evidence that pre-Hispanic
civilizations depended on the natural resources of

Correspondence: G. Pezzi, Department of Biological, Geological and Environmental Sciences, University of Bologna, Via Irnerio 42, IT-40126 Bologna, Italy.
Tel: 39 0512091302. Fax: 39 051242576. Email: giovanna.pezzi@unibo.it
q 2014 Societa` Botanica Italiana

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Plant composition along the Peruvian and Chilean fog oases


lomas is found in a few places such as the lomas of
southern Peru (Linares Malaga 1991; Cordero et al.
2009). In spite of their significance as diversity
hotspots, lomas are threatened by several human
activities such as coastal urbanization, intensive
agriculture, overgrazing, mining, and the collection
of fuel wood.
Lomas are characterized by a discontinuous and
fragmented distribution along the coast and are
differentiated from one another in their structure and
composition (Rundel & Mahu 1976; Muller 1985;
Rauh 1985; Dillon 1997; Cano et al. 1999; Cano
et al. 2001; Arakaki & Cano 2003; Dillon et al. 2003;
Pinto & Luebert 2009; Galan de Mera et al. 2011).
However, their biogeographical origin, together
with their current ecological relationships in terms of
species dispersal capability, remains an open question. While some authors support the hypothesis of a
biological connection between lomas (Ono 1986) or
the existence of a unique biogeographical region
along the coastal desert (Lopez et al. 2006) based
on the existence of a hypothetical ancient shared
bioclimatic scenario whose remnants can be sparsely
found today, some other authors emphasize the lack
of uniformity of the lomas of western South America
in terms of floristic composition (Duncan & Dillon
1991; Rundel et al. 1991; Rundel & Dillon 1998).
Differences were attributed to the desert barriers
found at , 188 198S between Chile and Peru (Galan

1003

de Mera et al. 1997; Dillon 2005) and at , 148S


between south and central Peru (Muller 1985; Galan
de Mera et al. 1997). In fact, the scarcity of common
species between Peruvian and Chilean lomas (ca.
7%, Rundel et al. 1991) has been attributed to the
presence of the desert barrier between South Peru
and Chile. Accordingly, to shed some insight into this
question, we examined the latitudinal pattern in
floristic and phylogenetic composition of 13 lomas
distributed from North Peru to North-Central Chile.
Data and methods
Thirteen lomas ranging from 78580 to 268150 S
(Figure 1), along the coasts of Peru (PE) and Chile
(CL), were selected for analysis. These lomas cover
the latitudinal extent of this habitat. Climate is
characterized by a long dry period (austral summer)
with a short and variable humid period (May
October) when fog is more frequent. A constant
hydric deficit affects the area throughout the year.
Annual precipitation is usually lower than 50 mm
with a minimum peak in Chile (2.5 7 mm). Climate
is highly influenced by El Nino Southern Oscillation,
which affects rainfall and fog intensity.
The lomas species lists were obtained from
available sources (Table I) and the LOMAFLOR
database, freely available at http://www.sacha.org/.
For the ferns, we referred to Leon et al. (2002) to fill

Figure 1. Geographic location of the analyzed lomas. Localities are coded as in Table I. CL, Chile; PE, Peru.

1004

R. Manrique et al.

Table I. List of the 13 lomas analyzed.


Code

Locality

Latitude (8S)

Longitude (8W)

Data sources

PE1
PE2
PE3
PE4
PE5
PE6
PE7
PE8
CL9
CL10
CL11
CL12
CL13

Cerro Campana
Lachay
Pachacamac
Atiquipa
Mollendo
Meja
Ilo
Tacna
Tarapaca
Morro Moreno
Quebrada Rinconada
Paposo
Pan de Azucar

78580 28.82
118190 45.41
128140 14.52
158460 54.02
168580 22.87
17860 32.83
178430 37.88
178470 42.38
208220 15.03
238290 58.82
248540 58.71
25810 18.51
26810 39.35

79860 53.22
778170 41.45
768500 7.30
748210 28.46
718590 56.89
718410 48.44
71890 4.41
71820 13.91
70870 48.54
708330 29.33
708280 28.64
708250 26.19
708360 34.19

LOMAFLOR
Cano et al. (1999); LOMAFLOR
LOMAFLOR
Jimenez (2006)
Jimenez (2006); LOMAFLOR
Puig et al. (2002); Jimenez (2006); LOMAFLOR
Arakaki and Cano (2003); LOMAFLOR
LOMAFLOR
Larran (2007)
Larran (2007)
Larran (2007)
Larran (2007); LOMAFLOR
Larran (2007); LOMAFLOR

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Note: CL, Chile; PE, Peru. The LOMAFLOR database is available at http://www.sacha.org/.

some gaps in the Peruvian inventories. Nomenclature follows Brako and Zarucchi (1993) and
Marticorena and Rodrguez (1995) updated according to Squeo et al. (2008).
The species life forms were classified into trees,
tall shrubs, small shrubs, cacti, lianas, perennial
herbs, annual herbs, and grasses. Because of the
heterogeneity of the Chilean and Peruvian sources,
we classified the species geographic origin into
endemic (i.e. species of coastal or Andean origin),
native (species from North, Central, and South
America), and introduced species.
The floristic relationships among lomas were
analyzed by nonmetric multidimensional scaling
(NMDS) of the species-by-site dissimilarity matrix
based on Jaccards dissimilarity. Species occurring
only at one site were removed from the analysis to
reduce random occurrences and to emphasize
similarities among sites. To relate the NMDS patterns
to the ecological characteristics of species, the vectors
of the species life form and origin were fitted as
variables onto the ordination. All multivariate
analyses were carried out with the Vegan package in
R version 2.10.1 (http://www.R-project.org).
To analyze the phylogenetic relationships among
lomas, we first constructed a time-calibrated phylogenetic tree of all angiosperms (i.e. , 97% of the
species in our list) using the software Phylomatic
(http://www.phylodiversity.net/phylomatic, Webb &
Donoghue 2005). We next calculated a matrix of
nearest neighbor phylogenetic dissimilarities
(NNPD) between lomas using the Phylocom software package (http://www.phylodiversity.net/phyl
ocom, Webb et al. 2008).
Given two sites, A and B, NNPD is the average
minimum phylogenetic distance between all species
in A and the species in B and vice versa:
P
P
i min d iB
j min d jA
NNPD
;
SA SB

where di B is the minimum phylogenetic distance


between species i in A and all species in B, and djA is
the minimum phylogenetic distance between species
j in B and all species in A. SA and SB are the number
of species in A and B, respectively. NNPD is thus a
measure of the average phylogenetic turnover
between each species in A and its phylogenetic
nearest neighbour in B and vice versa (Ricotta et al.
2012). High values of NNPD denote high phylogenetic turnover between sites, while low values of
NNPD imply high phylogenetic overlap between the
species in A and their nearest neighbours in B (for
mathematical details, see Izsak & Price 2001; Ricotta
& Burrascano 2008).
The phylogenetic dissimilarities among lomas
were finally analyzed with NMDS. Although the
phylogenetic trees constructed by Phylomatic usually
contain many polytomies at the genus and species
level, Phylomatic is one of the few freely available
programs that enable ecologists to reconstruct a
meaningful time-calibrated community phylogeny
for large and taxonomically heterogeneous species
assemblages like ours. Hence, we consider it an
acceptable, though suboptimal tool for integrating
phylogenetic data into studies of community ecology
and biogeography (Ricotta et al. 2013).
Results and discussion
Our inventory contains 1004 species belonging to
388 genera and 99 families, corresponding to
approximately 77% of the recorded species in the
region (Dillon 1997; Dillon & Hoffmann 1997;
Tago-Nakawaza & Dillon 1999). Species singletons
with only one occurrence in the 13 lomas accounted
for 56% of the whole species pool. Such high number
of single occurrences emphasizes the unique species
composition of individual lomas, which display
disharmonic patterns typical of true insular
communities (Dillon et al. 2003). Because of their

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Plant composition along the Peruvian and Chilean fog oases


ability to respond rapidly and opportunistically to
water pulses, most of the lomas plants are herbs (588
species, 59%), while endemics (230 species) represent 39% of the species pool.
The non-metric ordination of species presence
absence data (Figure 2) shows that, based on their
floristic composition, lomas outline a complex,
nonlinear latitudinal gradient in ordination space
arni et al. 2011). Along this gradient, the sites are
(C
grouped into three main clusters: North Peruvian
(PE1 PE3), South Peruvian (PE4 PE8), and
North-Central Chilean lomas (CL9 CL13). This
divergence among areas is consistent with previous
studies on Peruvian and Chilean floras (Muller 1985;
Duncan & Dillon 1991; Galan de Mera et al. 1997;
Tago-Nakawaza & Dillon 1999; Pinto & Luebert
2009). The same pattern is found with the ordination
of phylogenetic distances (Figure 3). However, in
Figure 3, the observed differences among the three
groups of lomas are smoother than in Figure 2. This
suggests that dissimilarity measures between species
assemblages are more comprehensive if based on all
taxonomic levels, not just species (Izsak & Price
2001), thus providing a higher degree of evolutionary
and biogeographic continuity to what looks like an
abrupt floristic change in Figure 2. Regardless of the
dissimilarity matrix used for ordination, significant
differences ( p , 0.05) were detected between the
three groups of lomas on both dissimilarity matrices

Figure 2. NMDS of species presences and absences (excluding the


species found only once) based on the Jaccard dissimilarity
coefficient (stress 5.875). The ordination plot shows the three
clusters of lomas, North Peruvian (PE1PE3), South Peruvian
(PE4 PE8), and North-Central Chilean lomas (CL9CL13),
together with the correlation of the species life forms (dashed
arrows), and geographic origin (continuous black arrows) with the
ordination axes. Vectors show the direction of the gradient; the
length of the arrows is proportional to the correlation between the
variable and the ordination axes.

1005

Figure 3. NMDS based on NNPD among lomas (stress 0.181).

using nonparametric multivariate analysis of variance


and 999 permutations (Anderson 2001).
Some insight into the floristic pattern observed in
the ordination space (Figure 2) is given by the
species life forms (Table II), which are probably
related to increasing aridity conditions from Peruvian
to Chilean lomas. For instance, lianas are more
abundant in northern Peruvian lomas, whereas cacti
and shrubs are mostly concentrated in the Chilean
lomas where aridity is higher (Galan de Mera et al.
2002; Lopez et al. 2006; Squeo et al. 2007; Galan de
Mera et al. 2009). In desert environments, shrubs
have an important function by acting as nurse plants
and performing a hydraulic lift action. The most
frequent shrub genera are Atriplex L., Bahia Lag.,
Croton L., Encelia Adans., Frankenia L., Heliotropium
L., and Nolana L.f. Similarly, while the selected
lomas include only a few tree species, such as
Caesalpinia spinosa (Molina) Kuntze and Myrcianthes
ferreyrae (Mc Vaugh), the higher presence of trees in
the Peruvian lomas differentiates them from the
vegetation of the Chilean group. Finally, as concerns
the species geographic origin, while our results show
a high degree of endemism in all lomas (e.g. out of 46
cacti in our checklist, 37 are endemics), the Chilean
group is characterized by an extraordinary richness in
endemic species (Dillon et al. 2003; Pinto & Luebert
2009), such that approximately one half of the
species in the North-Central Chilean lomas is of
coastal or Andean origin. This observation, together
with the poor species overlap between Peruvian and
Chilean lomas, reinforces the idea that, at least in
recent times, their floristic composition has been
shaped by barriers that limit the species dispersal
ability over long distances. For instance, while
molecular phylogenetic studies of different taxa,
such as Malesherbia Ruiz & Pav., Nasa Weigend,

Species number
Life forms (%)
Annual herbs
Perennial herbs
Grasses
Small shrubs
Tall shrubs
Trees
Cacti
Lianas
No info
Geographic origin (%)
Native
Endemic
Introduced
No info

137

40.15
32.85
7.30
2.92
9.49
0.73
0.73
4.38
1.46

64.23
24.09
9.49
2.19

20.71
37.28
8.88
5.33
13.02
1.78
2.96
7.69
2.37

69.23
24.26
4.73
1.78

PE2

169

PE1

67.57
20.72
9.91
1.80

39.64
37.84
2.70
1.80
7.21
0.90
2.70
6.31
0.90

111

PE3

North Peru

65.60
22.34
9.22
2.84

29.79
34.75
7.80
3.90
11.35
1.42
2.84
5.67
2.48

282

Tot

Table II. Main floristic attributes of the analyzed lomas.

50.00
25.00
16.67
8.33

30.88
34.80
7.84
3.43
8.33
1.96
2.94
2.94
6.86

204

PE4

50.96
36.94
6.37
5.73

33.76
34.39
8.28
3.82
8.28
1.27
3.18
0.64
6.37

157

PE5

50.00
31.43
10.00
8.57

34.29
28.57
11.43
2.86
10.00
1.43
1.43
0.00
10.00

70

PE6

60.00
20.95
14.29
4.76

41.90
35.24
9.52
1.90
2.86
1.90
0.00
2.86
3.81

105

PE7

South Peru

62.86
21.90
10.48
4.76

36.19
33.33
10.48
2.86
9.52
0.95
1.90
1.90
2.86

105

PE8

54.73
23.63
12.44
9.20

31.59
32.34
9.20
3.73
8.71
1.24
2.49
2.74
7.96

402

Tot

45.57
41.77
3.80
8.86

32.91
25.32
2.53
7.59
20.25
0.00
3.80
1.27
6.33

79

CL9

24.53
54.09
4.40
16.98

21.38
27.67
7.55
5.66
16.98
0.00
4.40
1.26
15.09

159

CL10

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32.99
56.70
7.22
3.09

25.77
36.08
1.03
3.09
24.74
1.03
2.06
3.09
3.09

97

CL11

38.62
51.01
9.80
0.58

36.31
26.51
8.93
3.75
15.85
0.58
4.90
2.59
0.58

347

CL12

North-Central Chile

30.15
65.83
3.02
1.01

26.13
27.64
8.54
5.03
21.61
0.00
8.54
2.01
0.50

199

CL13

33.98
50.39
8.11
7.53

30.69
25.68
8.30
5.02
15.64
0.39
5.98
1.93
6.37

518

Tot

44.02
38.65
9.16
8.17

29.58
28.98
8.57
4.88
12.35
1.00
4.58
2.99
7.07

1004

Entire dataset

1006
R. Manrique et al.

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Plant composition along the Peruvian and Chilean fog oases


Solanum L., Nolana, Heliotropium, or Polyachyrus
Lag. (see Pinto & Luebert 2009 and references
therein), support the existence of an ancient floristic
connection between the coastal regions of Peru and
Chile (Luebert & Wen 2008; Luebert 2011), the
observed floristic and phylogenetic differentiation
between the main groups of lomas (North Peru,
South Peru, and Chile) seems to support their
biological isolation, at least in recent times (Muller
1985; Galan de Mera et al. 1997, Dillon 2005). As
suggested by Galan de Mera et al. (1997), the
presence of two main desert barriers separating
North Peru from South Peru and South Peru from
Chile is a main source of isolation that limits species
migration and gene flow between these groups of
lomas. The ordination plots in Figures 2 and 3 seem
to support this viewpoint, rejecting the opposite
hypothesis on the presence of biological connections
that promoted the interchange and radiation of
species between southern Peru and northern Chile
(Ono 1986; Lopez et al. 2006), thus leading to one
unique biogeographical region along the Pacific
coastal deserts on South America.

Acknowledgements
The authors are grateful to the anonymous reviewers
for their very constructive comments and suggestions
to improve the quality of the paper.

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