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Ben-Gurion University of the Negev
The Jacob Blaustein Institutes for Desert Research
The Albert Katz International School for Desert Studies
Reducing the competitive load on desert bat communities by
hampering the drinking ability of an invasive bat species,
Kuhl’s pipistrelle (Pipistrellus kuhlii)
Thesis submitted in partial fulfillment of the requirements for the degree of
"Master of Science"
By: Asael Greenfeld
April 2012
Ben-Gurion University of the Negev
The Jacob Blaustein Institutes for Desert Research
The Albert Katz International School for Desert Studies
Reducing the competitive load on desert bat communities by
hampering the drinking ability of an invasive bat species,
Kuhl’s pipistrelle (Pipistrellus kuhlii)
Thesis submitted in partial fulfillment of the requirements for the degree of
"Master of Science"
By: Asael Greenfeld
Under the Supervision of Prof. David Saltz and Prof. Carmi Korine
Mitrani Department of Desert Ecology
Author's Signature …………….………………………
Approved by the Supervisor…………….……………..
Approved by the Director of the School ……………
Date …………….
Date …………….
Date ………….…
I
Reducing the competitive load on desert bat communities by
hampering the drinking ability of an invasive bat species, Kuhl’s
pipistrelle (Pipistrellus kuhlii)
By: Asael Greenfeld
This thesis is in partial fulfillment for the degree of Master of Science, Ben-Gurion
University of the Negev, Jacob Blaustein Institutes for Desert Research, Albert Katz
International School for Desert Studies, 2011
Abstract
Among the species comprising the bat community of the Negev desert in
Israel, three have expanded their range into the desert from Mediterranean habitats,
probably due to anthropogenic developments such as the addition of bodies of open
water and lights. The abundance and activity of bats in the desert is affected by the
distribution of bodies of open water, which are used by bats for drinking and foraging
sites. One of the species that has penetrated the Negev from Mediterranean habitats is
Kuhl’s pipistrelle (Pipistrellus kuhlii), the most common bat in Israel. Kuhl’s
pipistrelle competes for foraging habitats and food with three other species of bats
(P.rueppellii, Hypsugo bodenheimeri and Eptesicus bottae), comprising the
“background cluttered space” foraging guild. Kuhl’s pipistrelle drinks more
frequently than the other species of its guild and requires a clear “swoop zone” to
drink. I hypothesized that Kuhl’s pipistrelle uses newly established water bodies of
II
open to expand into desert habitats. To reduce the competitive load that Kuhl’s
pipistrelle has on desert dwelling species, I proposed and tested a management tool to
reduce the ability of Kuhl’s pipistrelle to drink from open bodies of water. I predicted
that, by installing obstructions above the water surface, I could reduce the drinking
ability of Kuhl’s pipistrelle, thus reducing their activity.
First, using acoustic methods, I surveyed natural and artificial bodies of open
water in the Ramon region in order to learn the current limits of Kuhl’s pipistrelle’s
range expansion and to study the mechanisms of its expansion. To study the effect of
obstructions on the water surface, I did field experiments. In each experiment, the
manipulation and control treatments were alternated, and the activity levels of the
different species present were monitored by acoustic methods.
I found in the survey that Kuhl’s pipistrelle are abundant in the Central Negev
Highlands, but absent from Makhtesh Ramon, and found activity levels of Kuhl’s
pipistrelle high in natural sites as well as in artificial ones. In the first field experiment
that tuck place in a swimming pool, I managed to prevent Kuhl’s pipistrelle's drinking
by obstructing the water surface and leaving just a 1x1m of “swoop zone”. In the
second manipulation experiment, in natural ponds in the Zin valley, I found that the
obstructions had no effect on activity levels or species composition. This might have
been the result of the proximity of untreated ponds to manipulated ponds in the study
area. In the third experiment, I chose isolated natural ponds throughout the Negev. I
found that, in some of the ponds, the manipulation significantly reduced Kuhl’s
pipistrelle activity. This reduction was observed in ponds that initially had higher
activity of Kuhl’s pipistrelle then of desert dwelling species.
III
I concluded that artificial bodies of open water may be part of the mechanism by
which Kuhl’s pipistrelle is expanding its range into the Negev. The existence of bodies of
open water pools in Makhtesh Ramon and the Southern Negev poses a risk of further
expansion of Kuhl’s pipistrelle into desert habitats from which they are currently absent.
With some further investigation of my predictions, manipulating artificial bodies of open
water could be used as a management tool to reduce competitive load from desert
dwelling species. Such a tool would be especially useful in the troughs established by the
National Parks Authority in the Negev, which were intended to facilitate biodiversity by
supporting wildlife, but are simultaneously threatening desert dwelling bat species.
IV
Acknowledgments
First and foremost I would like to thank my supervisors, Prof. Carmi Korine who
introduced me to the world of desert bats and invited me to continue my work at the
Ramon Science Centre and turn it into an M.S. research project, and Prof. David Saltz, for
giving me the opportunity to do this study under his supervision. I thank them both for
their advice, help and guidance throughout the planning, executing and writing of my
thesis.
I would have not been able to carry out my field work and experiments without
the help of many volunteers, neighbourhood friends and friends from the Libratory,
family members, and especially my students from the Mizpe Ramon Environmental
Studies Yeshiva high school. The pool experiment was performed with the help of two of
the course students: Keira Edwards and Ben Evans from the University of Bristol, UK.
I thank Noam Werner and Uri Shanas for lending me equipment, and Atlantis
Aquariums and the Alpaca Farm for their help with pool construction. I am also grateful
to the Israel Nature and National Parks Protection Authority for allowing me to carry out
my research in nature reserves, and individually, for all their help and advice, to: Ben
Drori, Nadav Tauba, Amram Tsabari, Gal Vine, and Assaf Tzoar.
Finally, nothing would come to be without the love and support of my beloved
wife Lea or without her smiles and those of our dear children, Rotem, Adi and Boaz.
My research was funded through grants from Ben-Gurion University Seed Money
to Carmi Korine and David Saltz, and from the Ministry of Technology and Science to
Carmi Korine. This work was supported through a scholarship from the Albert Katz
International School for Desert Studies.
V
Table of Contents
1. Chapter One - General Introduction.............................................................. 1
1.1 - Anthropogenic bodies of open water in desert environments and
their effect on local wildlife ....................................................... 1
1.2 - Diversity of insectivorous bats in association with water sources
.................................................................................................... 3
1.3 - The association between distribution of bodies of water and bats’
community structure in the Negev highlands ........................... 5
2. Chapter Two - Species composition of bat communities in different
habitats in the Ramon region, and the range expansion
mechanism of the Kuhl’s pipistrelle ...................................... 10
2.1 - Introduction ............................................................................... 10
2.2 - Methods ..................................................................................... 13
2.2.1 – Study area .................................................................... 13
2.2.2 – Survey species .............................................................. 15
2.2.3 – Field sampling methods .............................................. 17
2.2.4 – Data analysis of field sampling ................................... 20
2.3 - Results ...................................................................................... 21
2.3.1 – Total bat activity and Kuhl’s pipistrelle activity levels in
the different areas of the Ramon region ...................... 22
2.3.2 – Activity levels in the different site types .................... 25
2.4 - Discussion ................................................................................ 26
2.4.1 – Species composition of the “background-cluttered space”
guild in the Ramon region ........................................... 26
2.4.2 – Range expansion of Kuhl’s pipistrelle in the Ramon
region............................................................................ 28
3. Chapter Three - Managing bat community species composition by placing
obstructions to hamper the Kuhl’s pipistrelle ability to drink
from desert ponds ................................................................. 30
3.1 - Introduction ............................................................................... 30
3.1.1 – Management of alien invasive bat species .................. 30
VI
3.1.2 – Interspecific differences in the use of bodies of water as
the key for the management of desert bat communities 33
3.2 - Methods .................................................................................... 37
3.2.1 – Field experiment I: manipulation of the swimming pool
...................................................................................... 37
3.2.2 – Field experiment II: manipulation of natural ponds in the
Zin valley .................................................................... 40
3.2.3 – Field experiment III: manipulation of isolated natural
ponds ........................................................................... 44
3.3 – Field experiment results .......................................................... 48
3.3.1 – Manipulation of the swimming pool ........................... 48
3.3.2 – Manipulation of natural ponds in the Zin valley ......... 49
3.3.3 – Manipulation of isolated natural ponds ....................... 52
3.4 - Discussion ................................................................................ 55
3.4.1 – Manipulation of the swimming pool ........................... 55
3.4.2 – Manipulation of natural ponds in the Zin valley ......... 57
3.4.3 – Manipulation of isolated natural ponds ....................... 58
4. Chapter Four - General Discussion .............................................................. 60
4.1 - The current distribution of Kuhl’s pipistrelle, and its impact on
local bat communities ............................................................. 60
4.2 - The effect of pond manipulation on species composition ........ 61
4.3 - The potential use of the grid as a management tool for the Negev
bats ........................................................................................... 62
4.4 - Mitigation and Reconciliation rather than aggressive eradications
as the future of invasive species management ........................ 63
5. Chapter Five - Bibliography ..................................................................................... 65
VII
List of Figures
Chapter 2
Figure 2.1 - The known distribution of Pipistrellus kuhlii in the Negev (2009)…...… 11
Figure 2.2 – Map of field sampling sites in the Ramon region…………………….… 20
Figure 2.3 – Activity of Pipistrellus kuhlii in the Ramon region…………………….. 23
Figure 2.4 – Species composition in each area of the Ramon region………………… 24
Figure 2.5 – Genaral bat activity levels at different site types ………………………. 25
Chapter 3
Figure 3.1 - Diagram of the grid covering of the swimming pool experiment……….. 38
Figure 3.2 - Field experiment II – temporary pond sites in the Zin valley………….... 41
Figure 3.3 – An example of the network that was placed on pond surfaces………….. 43
Figure 3.4 – Map of sites for field experiment III in isolated ponds in the Negev........ 45
Figure 3.5 – Activity and drinking passes in the swimming pool experiment ……..…49
Figure 3.6 –Average bat activity levels in the different sites used for experiment III.. 53
Figure 3.7 – Pipistrellus kuhlii proportion in different treatments in experiment III .. 54
VIII
List of Tables
Chapter 2
Table 2.1 - Field sampling sites in the Ramon region………………………………… 19
Table 2.2 – Number of recordings from each survey site in the Ramon region……… 21
Table 2.3 – Activity of bat species at the survey sites in the Ramon region…………. 22
Chapter 3
Table 3.1 – Sites for experiment II in the Zin valley………………………………… 40
Table 3.2- Staggered use of ponds for experiment II in the Zin valley……….…….... 42
Table 3.3 – Sites for experiment III in isolated bodies of water………………...……. 45
Table 3.4 - Design of experiment III based on alternating the treatments……...……. 47
Table 3.6 – Bat activity at ponds in experiment II in the Zin valley………………….. 51
Table 3.7 – Regression slopes of proportions in experiment III……………………… 51
Table 3.8 – Activity of Pipistrellus kuhlii in experiment III......................................... 52
1
Chapter One - General Introduction
1.1 Anthropogenic bodies of open water in desert environments and their
effect on local wildlife
Man-made elements that influence water availability are having increasing
impact on arid ecosystems worldwide (Ragab and Prudhomme 2002). Arid and
semiarid landscapes are unique ecosystems where continual water availability
results in hotspots of biological diversity in an otherwise water-limited environment
(Noy-Meir 1973, Stromberg et al. 1996, Stromberg 2001). This results sharp special
differences between the vast xeric uplands and narrow mesic riparian environments
and by sharp temporal transitions (Stromberg et al. 1996).
Human development of arid and semiarid environments has, on the one hand,
lowered the water levels that support the base flow in some deserts by ground water
pumping which reduces the water availability to wildlife (Pool and Coes 1999), and
on the other hand, has created new water sources in many places, increasing the
water supply to desert fauna (O'Brien et al. 2006) and flora (Brooks et al. 2006). An
important type of anthropogenic water source is “water developments” used by
conservation authorities as an integral component in the maintenance and
enhancement of wildlife habitats in arid regions. In the deserts of the USA, there are
thousands of water developments (over 800 in Arizona alone), which go back as far
as the 1940s, intended to benefit game species and other wildlife (Rosenstock et al.
1999). Contemporary water developments are now constructed in the USA to
accommodate use by a variety of wildlife and to mitigate the loss of natural water
sources (Rosenstock et al. 2004).
2
The importance of bodies of open water to wildlife increases during the dry
season, and visits to anthropogenic bodies of open water by birds and mammals
intensify with the rise in Ta (O'Brien et al. 2006). There has long been a
controversy regarding the effects of water developments on local wildlife, in which
critics argue that these developments do not yield expected benefits to game species
and may have adverse impacts, such as affecting prey species by localizing
predation (O'Brien et al. 2006). Additionally, the use of water for agriculture,
sewage treatment, and recreational reservoirs affects the distribution of local
wildlife and enhances the successful introduction and spread of invasive species
(Griffin 1998, Dukes and Mooney 2004, Lobos et al. 2005).
In recent years, the increase in human population and the concomitant increase
of inland agricultural development in Israel have had strong negative effects on
many vertebrate species (Yom-Tov and Mendelssohn 1988). In the Negev Desert,
agricultural development has brought about an increase in the number of bodies of
open water, mostly by collecting ground water in reservoirs (Portnov and Safriel
2004). An important type of water development in the Negev is construction of
artificial water troughs for wildlife, first used in the 1990s to support the
reintroduced population of Asiatic wild ass (Equus hemionus) (Saltz and
Rubenstein 1995). Water developments in the Negev affect the distribution of
wildlife and promote invasion by invasive species and the range expansion of others
(Hawlena and Bouskila 2006). Invasive alien species have been found harmful to
local native communities by means of resource competition with the local species,
increased predation on the local prey communities, and the introduction of
pathogens and parasites that may threaten local fauna (Simberloff 2010). Thus, the
3
invasion of alien Mediterranean species into the desert wildlife community may
have a negative impact on local populations.
1.2 Diversity of insectivorous bats in association with water sources
Among terrestrial mammals, bats play key roles in temperate and tropical
ecosystems. This is due to their large number of species (species richness),
enormous numbers of individuals, mobility, geographical distribution, and their
important functions as seed dispersers, pollinators, and arthropod predators (Hill
and Smith 1984). The activity level of insectivorous bats varies in time and space
and is associated with several factors that have been well studied. Of these factors,
those influencing the abundance of insects are of primary importance because the
choice of foraging site is directly linked to food availability (Rydell 1992), the
length of foraging bouts (Swift 1980), and the time of parturition (Kunz 1973,
Arlettaz et al. 2000). Many studies report that insect activity is directly proportional
to ambient temperature (Ta), and consequently, at low Ta, bat activity is reduced
(Williams 1961, Bradley 1970, Rydell 1989, Wai-Ping and Fenton 1989, O'Farrell
and Hayes 1997) and it is higher during the summer (O'Farrell and Bradley 1970,
Seidman and Zabel 2001, Korine and Pinshow 2004, Adams and Thibault 2006).
Bodies of open water also play a key role in bat distribution and habitat
preference since they are used by bats as a source of drinking water and as foraging
areas (Vaughan 1996, Grindal et al. 1999, Ciechanowski 2002, Razgour et al.
2010). The importance of drinking is demonstrated by Webb et al. (1995), who
report immense water loss, up to 30% of a bat’s body mass in Plecotus auritus and
Myotis daubentoni, two non-desert species, during one day while resting. Since
4
bats drink in flight, their drinking behavior depends on their flight performance
(Norberg and Rayner 1987). Flight performance, in turn, is a combined product of
wing morphology and mechanical properties of the wing membrane and bones.
These attributes vary considerably among bats (Swartz et al. 2004). Bats that can
hover can drink from almost any size of water body, while high speed flyers require
an unobstructed ‘swoop zone’ (Harvey et al. 1999), and consequently, can drink
from smaller and from more obstructed bodies of water, than larger bats (Tuttle et
al. 2006). Insectivorous bats likely prefer hunting over open water because the
echoes of insect bodies are reflected from the water surface and provide a stronger
target than similar size prey in the open air (Siemers et al.2001). In a recent study
(Jackrel and Matlack 2010) demonstrated how the drinking preferences of bats from
artificial water tanks follow the physical properties of the water source. The authors
found that bats drink more frequently from larger tanks (diameter = 3 m) than from
smaller tanks (d = 1.2 m), from full tanks more than from half-full tanks, and that
bats prefer tanks with less surrounding vegetation. All three criteria affected the
drinking frequency, but not the total flight activity, suggesting that all tanks were
equally suitable as foraging areas. Bat activity and species richness increase with
pond size, and temporary ponds do not significantly differ from permanent ones in
activity levels (Razgour et al. 2010). High levels of bat activity are consistently
found over open water (Rydell et al. 1994, Walsh and Harris 1996, Vaughan et al.
1997, Russo and Jones 2003), including in the Negev desert (Korine and Pinshow
2004). The importance of open water bodies was further demonstrated by Greif and
Siemers (2010), who showed that the recognition of bodies of water by the bats is
innate. Their experiments may indicate that bats have evolved the adaptation to
5
innately locate water in complete darkness, allowing even juveniles, which have
never before encountered an open body of water, to identify it as a source of
drinking water by echolocating its smooth surface.
1.3 The association between distribution of bodies of water and bats’
community structure in the Negev highlands
The availability of open bodies of water plays a key role in determining the
abundance and composition of bat communities in specific habitats. The proximity
to water was found to be an important factor in the choice of diurnal roosts by
species of bats in semi-arid northern Arizona (Rabe et al. 1998), while similar
studies done in wetter climates in Oregon (Betts 1998, Waldien 1998) found no
such effect. However, other studies found no effect of water availability on roost
preference, although night activity levels were higher near bodies of water (Waldien
1998). Since different species vary in their water requirements (Razgour et al.
2010), the abundance and nature of open bodies of water are expected to influence
species composition, especially in desert bat communities. The link between water
distribution and community structure has been studied in Poland (Ciechanowski
2002, Mysłajek et al. 2007) and, recently, in the Negev desert by Razgour et al.
(2010). In the mesic Polish forest, smaller ponds have higher species richness than
larger ponds or rivers. This was explained by the fact that, in ponds, the habitat
requirements of both water-obligated foragers and of dense vegetation foragers are
met (Ciechanowski 2002, Mysłajek et al. 2007). In the Negev desert, on the other
hand, bat species richness and activity are inversely proportional to pond size
(Razgour et al. 2010). Razgour et al. (2010) also report that, while total bat activity
6
is not affected by the hydro-period (the time that ponds hold water) of a pond, the
bat community composition differs between permanent and temporary ponds. Nondesert bat species were found to drink more frequently at larger ponds either
permanent, or with lengthy hydro-periods. Pond size also affects bat community
structure based on species maneuverability, with larger species avoiding smaller
ponds (Ciechanowski 2002, Razgour et al. 2010).
Insectivorous bats are among the species most affected by anthropogenic
disturbances to natural habitats (Yom-Tov and Mendelssohn 1988), and it seems
that, in some cases, modification of the natural environment causes changes in bat
community structure, resulting in competitive exclusion of some species. Arlettaz et
al. (2000) suggest that artificial foraging sites facilitated the expansion of common
pipistrelle (Pipistrellus pipistrellus) populations in the Swiss Alps. This apparently
resulted in competition with the lesser horseshoe bat (Rhinolophus hipposideros),
contributing to a decline in the population size of the latter. High levels of bat
activity in artificial sites in the Negev Desert are linked with lower bat species
richness (Korine and Pinshow 2004). Similarly, urban parks with lakes were found
to support fewer bats and less diverse bat communities than those close to rural
lakes (Kurta and Teramino 1992).
Of the 34 insectivorous bat species found in Israel, 12 inhabit the Negev Desert
(Korine and Pinshow 2004). Nine of the 12 Negev bat species are associated with
arid areas, and the other three -- Kuhl's pipistrelle, the European free-tailed bat
(Tadarida teniotis), and the rare lesser horseshoe bat (Rhinolophus hipposideros) -are invasive Mediterranean species that have expanded their distribution into the
Negev in the 20th century (Yom-Tov and Mendelssohn 1988, Yom-Tov and
7
Kadmon 1998). Kuhl's pipistrelle, one of these Mediterranean species, shares the
same guild with three other local species: Ruppell's pipistrelle (P. rueppellii),
Bodenheimer's pipistrelle (Hypsugo bodenheimeri) and Botta's serotine (Eptesicus
bottae). All four have similar diets of flying insects, mainly Lepidoptera (Whitaker
et al. 1994, Feldman et al. 2000), have similar wing morphology and forage in
similar habitats (Korine and Pinshow 2004). The four species belong to the same
guild as defined by wing and ear morphology (Yom-Tov 1993), and also by habitat,
as defined by Korine and Pinshow (2004), who named them the “backgroundcluttered space” guild, after their preferred foraging habitat. Kuhl's pipistrelle,
Ruppell's pipistrelle, and Bodenheimer's pipistrelle evidently compete over the use
of ponds for drinking and foraging, resulting in temporal and spatial partitioning
between these species (Razgour et al. 2011). These authors also report that Kuhl's
pipistrelle prefers smaller ponds and, when competitors are present, its activity
peaks several hours after sunset; Ruppell's pipistrelle prefers medium-sized ponds
and its activity peaks after sunset and before sunrise, in the presence of competition;
and that Bodenheimer's pipistrelle prefers larger ponds, where its activity peaks
three hours after sunset. On a seasonal scale, the increase in the size of the
competing populations of Ruppell’s pipistrelle and Bodenheimer’s pipistrelle, in
autumn and spring, was correlated with a decrease in the presence of Kuhl’s
pipistrelle at ponds frequented by the two other species (Razgour et al. 2010). While
these findings do not prove competitive displacement, they do suggest incomplete
resource partitioning that leads to competition. Accessibility to drinking water is
probably the limiting factor for the use of smaller ponds, and Mediterranean species
8
that drink most frequently were found to be associated with larger, permanent ponds
(Razgour et al. 2010).
Kuhl’s pipistrelle has expanded its range following human development (YomTov and Mendelssohn 1988). Artificial bodies of open water in the Negev highlands
were found to be used mainly by two species of bats: Kuhl’s pipistrelle and the
European free-tailed bat. These species are the two most common insectivorous bat
species in Israel (Yom-Tov and Mendelssohn 1988) and are closely associated with
human habitats in the Negev (Korine and Pinshow 2004).
The documented competition of Kuhl’s pipistrelle with the desert-dwelling
Ruppell’s pipistrelle and Bodenheimer’s pipistrelle that are restricted to only a few
foraging areas (Razgour et. al 2010), combined with the increasing development of
new bodies of open water in the Negev, raises two conservation-related concerns
regarding local bat biodiversity:
1) Mediterranean bat species, such as Kuhl’s pipistrelle, may further expand
their distribution and penetrate into even the more rural habitats, bringing with them
possible resource competition, introduction of pathogens and parasites and other
problems associated with invasive species.
2) In areas where Kuhl’s pipistrelle populations are already established, they
may change the local species composition by means of competitive exclusion of
other members of the guild. Ruppell’s pipistrelle and Bodenheimer’s pipistrelle are
classified as regionally endangered (EN), and Botta's serotine as vulnerable (VU)
(Dolev and Perevolotsky 2004), implying that any decrease in populations of these
species would be harmful to regional biodiversity.
9
The main goal of my research was to address these two concerns by:
1) Exploring the more Southern parts of the Negev highlands, which were
unexplored in terms of bat communities. Accordingly, I made a survey in which I
determining the possible boundaries of the current range of Kuhl’s pipistrelle in this
region.
2) Experimentally assessing the feasibility of a management tool which I
propose, namely hampering the drinking ability of Kuhl’s pipistrelle from bodies of
water by limiting the available “swoop zone.” This was done in an attempt to create
“protected habitats” for desert-dwelling bats, in order to reduce the competitive use
of bodies of water by Kuhl’s pipistrelle and the desert-dwelling species of its
feeding guild.
10
2 Chapter Two – Species composition of bat communities in different habitats
in the Ramon region, and the range expansion mechanism of the Kuhl’s
pipistrelle
2.1 Introduction
The dispersal of Kuhl’s pipistrelle into the Negev was first observed by YomTov and Mendelssohn (1988) and supported by the results of a cluster analysis of
their distribution by Yom-Tov and Kadmon (1998), yet the limits of this range
expansion are not clear. Most of the available data regarding species distribution in
desert habitats in Israel were, until the late nineties, collected from the Dead Sea
area and the Arava rift valley (Yom-Tov and Kadmon 1998).Yom Tov and Kadmon
(1998) created a model predicting the regional distribution of bat species. The
model is based on temperature and annual precipitation, and they predicted the
presence of Kuhl’s pipistrelle throughout the entire Negev. The model does not
take into account other local scale elements, such as water availability or interspecies interactions. In a later study of the insectivorous bat community of the
northern Negev highlands, Kuhl’s pipistrelle was found to be highly abundant in all
natural and man-modified sites surveyed as far South as the Zin Valley (Korine and
Pinshow 2004). Their data, together with accumulated unpublished data (Korine
personal communication and the SPNI database of 2011 that reports observations
collected by the Society for the Protection of Nature in Israel, on the abundance of
Kuhl’s pipistrelle in the Arava, covered most of the more developed regions of the
Negev (see Figure 2.1), but left an information gap comprising the whole southern
11
Negev, including the Ramon ridge, with only a vague indication of the extent to
which Kuhl’s pipistrelle has penetrated this rural area. Incidental observations
reported in the SPNI database 1122 report Kuhl’s pipistrelle in the Paran valley
(1991), in Mitzpe Ramon (1991), at the Hemet and Lotz cisterns and Ein Hava
(1994, 1996), and once at Ein Saharonim (1994). The first published report of the
capture of a Kuhl’s pipistrelle in Eilat was in 2002 (Zelenova and Yosef 2003).
More recently reports of Kuhl's pipistrelle in Eilat have become common in the
International Birding and Research Centre, Eilat area (Shalmon, personal
communication). Benda et al. (2008) surveyed the Sinai Peninsula and found no
evidence of further expansion into the Sinai. The importance of the Ramon region,
compared with the northern Negev and the Arava, is that it comprises the largest
portions of undeveloped wilderness in Israel, with some of the largest nature
reserves in the country, such as the “Tzinim Cliffs” and the “Har Hanegev”
reserves. Many of the areas, in addition to being
declared nature reserves, are further protected from
development by serving as military training zones (Tal
2008). This makes them important as wildlife refuges,
protecting desert species from the habitat modification
caused by the residential and agricultural development
Northern Negev
occurring in the rest of the Negev (Mazor 2001).
Figure 2.1 – The known distribution of Pipistrellus kuhlii in
the Negev prior the survey (dots) was limited to the Northern
Negev and the Arava, and anecdotal observations in the
Ramon region and southern Negev. Map based on BioGIS (2012)
Southern
Negev
12
Korine and Pinshow (2004) suggested that bat populations are affected by the
creation of artificial feeding and drinking sites in desert habitats. They based this
contention on the fact that they recorded the highest activity levels of bats at
artificial sites, and that Kuhl’s pipistrelle and the European free-tailed bat were the
only species that were abundant at these sites.
Artificial sites in the Ramon region are of two sources: 1) In towns and
agricultural settlements (limited to the town of Mitzpe Ramon, and some small
farms along Road 40 leading to the town). Mitzpe Ramon and the small farms have
water treatment, swimming pools and artificial lights, all of which cause insects to
congregate. Several army camps are located within the region and produce similar
modifications of their surroundings. 2) Artificial watering troughs, built to support
biodiversity of large animals, are also a potential threat to bat biodiversity since
they may support the invasion of alien bat species that may eventually reduce bat
biodiversity. Yet, there has been no monitoring of these troughs, as far as bats are
concerned (NPA rangers, personal communication).
One goal of my research was to achieve a better understanding of the role that
artificial ponds may play in the mechanism by which Kuhl’s pipistrelle expand their
range into desert habitats. This was done by studying the distribution of the bats at
the edge of their range along their suspected expansion front, the Ramon region.
Along with the abundance of Kuhl’s pipistrelle, I also monitored the abundance of
the other members of the “background-cluttered space” guild, Botta's serotine,
Ruppell’s pipistrelle and Bodenheimer’s pipistrelle, to explore understand possible
competition or coexistence within this guild (Korine and Pinshow 2004). I also
studied the effect of water availability on the activity levels of the abovementioned
13
species. I hypothesized that the distribution of Mediterranean insectivorous bats in
desert habitats is influenced by anthropogenic activities. This led to the following
predictions:
1) On the regional scale, Kuhl’s pipistrelle is more abundant in areas with
anthropogenic disturbances, such as residential and military development, than in
the rural areas, leading to differences in the species composition of bats among the
areas.
2) On the local scale, Kuhl’s pipistrelle activity levels are higher near artificial
water sources than near ephemeral natural water sources, and newly established
water source will attract Kuhl’s pipistrelle and therefore their activity level will
increase.
3) Where bodies of open water are available, a larger proportion of the total bat
activity is that of Kuhl’s pipistrelle, than of desert-dwelling species. At sites far
from bodies of open water, a higher proportion of the total bat activity is of desertdwelling species then of Kuhl’s pipistrelle.
2.2 Methods
2.2.1 Study area
Field sampling of bat community compositions took place in areas that are
estimated to be the front edges of expansion for the Mediterranean bat species, i.e.
the Ramon region. The 200 m high Makhtesh Ramon south-facing cliff, extends
over 40 km from the North-East (3069’N, 3495’E) to the South-West (3050’N,
3464’E). The cliff is a natural boundary between two climatic zones, arid at the top
(700 m -1000m above sea level) and hyper-arid in the lower part of the
14
Makhtesh(450 m - 550 m above sea level), and is also the southern edge of
agricultural and water developments in the Negev highlands (Mazor 2001).
Incidental observations and preliminary recordings indicated that the Mediterranean
bat species are present north of the cliff but not south of it (Korine unpublished data
2008, BioGis 2012). In this desert region rain occurs during winter with large
annual differences in total precipitation and in its temporal and spatial distribution.
Ta are highest during summer and are lowest in winter, with a daily mean of 25 °C
in August, and 10-11 °C in January (Hillel and Tadmor, 1962).
Bodies of open water in the Ramon region are limited, and most of them are
associated with human activity. The region can be divided into three areas (Fig 2.2),
based on climatic and ecological differences between them, following Ward et al.
(2000):
A. Central Negev Highlands
This area consists of the highest mountaintops in the Negev region (Ramon
Mountain - 1071 m), with occasional snow during some winters. These mountains
are the origin of the big wadis that drain the entire area (Zin, Nitzana, Ramon). The
area has been found to receive more annual rainfall (100 mm) than its surroundings
(Ward and Olsvig-Whittaker, 1993). The area is unpopulated and uncultivated, and
the only sources of anthropogenic disturbances to wildlife are limited to hiking,
military camps, and military activity.
B. Mitzpe Ramon and its surroundings
The town of Mitzpe Ramon was established on the northern cliff of Makhtesh
Ramon and is part of the Central Negev highlands, with a slightly lower altitude
(880-900m) the their western side. This is an area with higher density of human
15
development than the Makhtesh and the rest of the Central Negev Highlands. The
town of Mitzpe Ramon and the surrounding farms and water developments create
an artificial oasis of modified habitat, in extreme contrast to the arid landscape
surrounding it.
C. Makhtesh Ramon
This area is much lower (from 800 m and down to 420 m) and drier than the rest
of the Ramon region, with an average of 56 mm of precipitation per year in the
eastern, lower part, and up to 80 mm average annual precipitation at the western
edge (Ward and Olsvig-Whittaker 1993). The vegetation is limited to the wadis.
The area is unpopulated with no agriculture, and most of it is a nature reserve with
limited hiking trails and dirt roads (Mazor 2001).
2.2.2 Surveyed species
In the field, all bats species were recorded, but the following three species -Kuhl’s pipistrelle, Bodenheimer’s pipistrelle, Botta's serotine that belong to the
“background-cluttered foraging" guild (Korine and Pinshow 2004) were the focus
of my research. The fourth member of this guild, Rueppell’s pipistrelle, was never
recorded In the Ramon region. Since Rueppell’s pipistrelle is not easy to
differentiate acoustically from Bodenheimer’s pipistrelle, I chose to neglect the
possibility that an occasional individual was present in my study sits and it’s passes
were counted as though it was a Bodenheimer’s pipistrelle.
A. Kuhl’s pipistrelle (Pipistrellus kuhlii) – family Vespertilionidae, subfamily
Vespertilioninae. It is a small (body mass ~ 6.5-7.5 g) and common insectivorous
bat, and it occurs in a wide variety of natural and anthropogenic habitats from
16
southwest Asia to southern and eastern Africa. In Israel, it is the most common bat
and is found from the north of the rift valley and Mediterranean down to Eilat and
in some desert habitats (Yom-Tov and Kadmon 1998). It is an aerial forager,
tending to use artificial lights and bodies of water for foraging (Korine and
Pinshow 2004). Most of its activity occurs in the early hours of the evening.
Echolocation calls used by this bat while foraging are most intense at around 3540 kHz (Whitaker et al. 1994, Berger-Tal et al. 2008).
B. Bodenheimer’s pipistrelle (Hypsugo bodenheimeri) – family
Vespertilionidae, subfamily Vespertilioninae. It is the smallest bat species in Israel
(body mass 2.5-2.9 g). It occurs in the desert regions of Arabia and Egypt (Benda
et al. 2008), and in Israel, it is found in the rift valley from Ein Geddi to Eilat and
in the southern Negev (Yom-Tov and Mendelssohn 1988). It is an aerial forager
that tends to fly low over the ground, around trees and, mainly around bodies of
water. Most activity occurs in the early hours of the evening. The echolocation
calls of this bat are most intense at around 44-46 kHz (Whitaker et al. 1994,
Riskin 2009).
C. Botta's serotine (Eptesicus bottae)- family Vespertilionidae, subfamily
Vespertilioninae. It is a small/medium-sized (body mass 7-9 g) insectivorous bat.
It occurs in dry habitats, from India and western China to Egypt and the Eastern
Mediterranean (Benda et al. 2008), and is found in Israel from the north of the rift
valley down to Eilat and the Negev Desert (Yom-Tov and Mendelssohn 1988). It
is an aerial forager, commonly foraging above vegetation (Korine and Pinshow
2004). The echolocation calls of this bat are most intense around 32-33 kHz
(Benda et al. 2008, Holderied et al. 2005).
17
2.2.3 Field sampling methods
I measured the activity levels of the different bat species by sampling their
echolocation calls, using Bat detectors (AnaBat II, Titley Electronics, Australia). I
defined bat activity as the number of bat passes per hour of recording at each
pond, whereby a pass is a sequence of bat calls (Fenton 1970). The echolocation
call frequencies of the bat species found in the Negev do not overlap (Benda et al.
2008). Therefore, I was able to distinguish individual calls at the species level.
Only echolocation calls emitted during foraging were used to distinguish between
the species and to determine activity levels for each species.
I studied the bat community compositions in each of the three areas, Makhtesh
Ramon, the Central Negev Highlands and the Mitzpe Ramon area. In each area, I
sampled three locations, which represent three different habitats (Table 2.1): natural
sources of water such as water holes, artificial bodies of water (see description
below), and, as a control, wadis without any known source of water but with
vegetation cover. Due to the extremely dry winter of 2008-2009, with only 50% of
the annual mean precipitation and the last rain event occurring in March, all the
natural water sources surveyed did not contain ponds throughout the entire survey.
Natural water sources were expected to attract high bat activity levels even without
water, due to the fact that they were surrounded by dense vegetation. Sites
surrounded by dense vegetation, studied by Korine and Pinshow (2004) have higher
bat activity levels compared with the sites categorized as dry sites.
Sampling locations were chosen based on the home ranges of similar bat
species, Common pipistrelle and the Soprano pipistrelle, that were found to forage
up to 2-3 km away from their roosts, and never more than 3.8 km away (Nicholls
18
and Racey 2006). These distances were recorded for non-desert species in Great
Britain, a fact that may affect their relevance to my study, yet they allow a rough
estimate of commuting distances. To lower the probability that bats from the same
populations would be recorded in different areas, I made sure that the distances
among the areas exceed 8 km, namely, more than twice the maximum estimated
commuting range of Kuhl’s pipistrelle. The distances between the sites within areas
were chosen to exceed 3 km to minimize the probability of counting the same bat at
two sites in one night. All sampling sites were located in wadis with dense
vegetation compared to the surrounding slopes.
One new artificial pool was built in the Mitzpe Ramon area, within the vicinity
of the Alpaca farm (30°36'36"N, 34°46'39"E). The other two artificial pools that
already existed in Makhtesh Ramon and the Negev highlands north of Mitzpe
Ramon (NPA troughs) were reconstructed to the same dimensions, thus controlling
for pond characteristics (shape and size) that may affect bat activity (Razgour et al.
2010). They were all located at ground level, rectangular in shape, and 3  2.5 m
minimal size. To construct the pools, I dug 30-50 cm deep ditches and covered
them with 0.8 mm thick, black P.V.C sheets (Sera GmbH,Heinsberg, Germany).
The water level was kept 20-30 cm deep using a valve with a float, allowing inflow
to compensate for evaporation.
Each site was sampled at least three nights in each of three seasons during 2009:
spring (March-May), summer (June-August), and fall (September-November), from
dusk (17:45-19:00, GMT+2) to dawn (04:30-05:45). In 2010 and 2011, partial
sampling was performed at the artificial site in the Alpaca farm. All sampling nights
took place during and close to the new moon, to prevent possible bias caused by the
19
increased lunar illumination that reduces bat activity, as was reported for some
species (reviewed by Lang et al. 2006). Each sampling night consisted of recording
bat calls using an AnaBat detector, positioned at a distance of approximately 5 m
from the pond at a vertical angle of 45°, and measuring proximate Ta (±0.5 °C)
every hour using iButton® data loggers (Dallas Semiconductor, Maxim Integrated
Circuits, Dallas, USA), which were sensitive. iButtons were placed approximately
1m above the ground, sheltered within vegetation from the wind.
Table 2.1- Field sampling sites in the Ramon region, Israel. Sites were designed to cover
the three different areas by surveying three types of sites in each area.
Natural
water
sources
Dry
Wadis
Makhtesh Ramon
1. Saharonim – A natural
spring. 30°36'13.22"N
34°56'14.11"E
2. Ramon – On the banks
of the eastern Ramon
Wadi. 30°36'58.87"N
34°55'18.85"E
Artificial 3. Afor - An NPA trough
bodies of in the Afor Wadi.
30°36'44.98"N
water
34°54'39.87"E
High Negev Mountain
4. Lotz – One of the
Borot Lotz cisterns.
30°30'22.56"N
34°36'45.64"E
5. Dorban – A tributary
of the Nitzana Wadi.
30°33'8.97"N
34°38'59.91"E
6. Nitzana – An NPA
trough in the Nitzana
Wadi.
30°32'32.30"N
34°38'43.40"E
Mitzpe Ramon area
7. Hemet – A cistern
8 km west of the
town. 30°35'36.85"N
34°42'35.73"E
8. Zin – On a tributary
of the Zin Wadi, 6 km
west of the town.
30°35'59.78"N
34°45'12.61"E
9. Alpaca farm – A
pool set up for the
experiment.
30°36'36.11"N
34°46'39.07"E
20
10 Km
Mitzpe Ramon area
Makhtesh Ramon
Central Negev Highlands
Figure 2.2 - Field sampling sites in the Ramon region: Makhtesh Ramon area (1-3), Central Negev
Highlands (4-6), Mitzpe Ramon area (7-9). The different site types are represented by colors:
natural water sources (green), dry wadis (red), and artificial bodies of water (blue). The broken line
represents the northern cliff of Makhtesh Ramon.
2.2.4 Data analysis of field sampling
I analyzed the calls using the software AnalookW 3.3q. Each AnaBat recording
file contains at least one bat pass. I counted the number of passes for each species
for each night and standardized the data by dividing the total passes for each night
by the number of hours from dusk to dawn. Since the activity levels for all species
were not normally distributed and their among-group variance lacked homogeneity,
and since many ‘0’ values were recorded, some of the statistical tests required
21
log(x+1) transformation and the use of non-parametric statistics. I used the multivariant statistics “one way ANOSIM” which is a tool that uses non-parametric
multi-dimensional scaling (nMDS) to present the degree of similarity compared to a
null hypothesis of identity. 0 < R < 1 is defined as the degree of similarity, and
ranks from R = 0 (different) to R = 1 (identical). I used ANOSIM to test the
differences between the species compositions in different areas with PAST software
(Hammer et al. 2001). All other analyses were done with STATISTICA7 software.
Results were considered significant at p < 0.05.
2.3 Results
Bat recordings were obtained from nine sites, during 10 months (FebruaryNovember) in 2009. Data from ten nights were lost due to vandalizing of equipment
or technical problems. Therefore, data are available from 80 full night recordings
(Table 2.2). Distribution of sampling nights between seasons was even, except for
the Zin site where data for the spring was lost. Partial recordings continued in 2010
and 2011 at the Alpaca farm for studying the long term effects of the new water
source.
Table 2.2 – The number of night recordings for which data were available from
each site during survey of 2009 in the Ramon region, Israel:
Central Negev
Mitzpe Ramon
Makhtesh
Total nights
Highlands
area
Ramon
per site type
Lotz
Hemet
Saharonim
25
Natural
7
9
9
Nitzana
Alpaca farm
Afor
30
Artificial
11
9
10
Dorban
Zin
Ramon
25
Wadi without
10
6
9
water
28
24
28
Total per Area
80
22
2.3.1 Total bat activity and the activity level of Kuhl’s pipistrelle in the
Ramon region
Activity varied considerably among nights and sites (min = 0, max = 59.88).
Variations among the different sites were considerable (max in Afor = 14.59, and
min in Zin = 0.03, Mann–Whitney U-test, p = 0.0048, Table 2.3). Total activity was
positively correlated with Ta (Spearman rank correlation: r2 = 0.4, p = 0.0002).
Table 2.3 – Activity levels of Pipistrellus kuhlii, Eptesicus bottae, Hypsugo
bodenheimeri at each of the 2009 survey sites in the Ramon region, Israel.
Activity is presented in average pass per hour ±SD.
Area
A. Makhtesh
Ramon
B. Central
Negev
HIghlands
C. Mitzpe
Ramon area
Site name
P. kuhlii
E.bottae
H. bodenheimeri
1.Saharonim
2. Ramon
3. Afor
4. Lotz
5. Dorban
6. Nitzana
7. Hemet
8. Zin
9. Alpaca
Total
0
0
0.06±0.08
0.14±0.16
2.13±4.01
8.64±15.02
1.82±2.63
0.015±0.037
0.013±0.04
1.68±6.29
2.68±3.21
0.16±0.29
3.67±3.94
0
0
0.18±0.50
0.14±0.26
0.02±0.05
0.05±0.09
0.83±2.17
5.43±4.56
1.45±2.11
10.88±17.51
0
0.01±0.03
1.20±3.91
0.03±0.06
0
0.01±0.03
2.305±7.27
Kuhl’s pipistrelle was highly active in the areas of the Central Negev Highlands
(mean activity level= 4.19 ± 10.14 pass/hour), less so at the Mitzpe Ramon sites
(0.67 ± 1.79), and nearly absent from the Makhtesh sites (0.02 ± 0.05). In fact, only
two Kuhl’s pipistrelle passes were recorded with certainty south of the Makhtesh
cliff during the entire year of the survey and in additional recordings during the
following year (Table 2.3 and Figure 2.3). The differences between the Central
Negev Highlands and the Makhtesh areas were significant (two-tailed Kruskal-
23
Wallis ANOVA on transformed data: H1,55 =16.90, p = 0.0003). The differences
between the Central Negev Highlands and Mitzpe Ramon were also significant
(H1,51 = 6.42, p = 0.019), but the differences were not significant between Mitzpe
Ramon and the Makhtesh (H1,51= 2.07, p = 0.30).
8
A
7
6
4
3
/
hour
/ hour
Passes
Passes
5
B
B
2
1
0
Central Negev Highlands Mitzpe Ramon area
Makhtesh Ramon
Area
Figure 2.3 – Average activity levels ±SD of Pipistrellus kuhlii throughout
the survey in the three different areas of the Ramon region, Israel. Different
letters above bars indicate significant differences (Kruskal-Wallis ANOVA
p< 0.02).
Species composition was significantly different between the High Negev
Mountains and the Makhtesh Ramon (one-way ANOSIM: p < 0.002, R = 0.73).
Kuhl’s pipistrelle dominated the Central Negev Highlands community and was
absent from the Makhtesh, while Bodenheimer’s pipistrelle dominated the
Makhtesh community and was less common in the Central Negev Highlands and
Mitzpe Ramon areas. The community of the Mitzpe Ramon area was intermediate
24
in the proportion of each species between the Central Negev Highlands and
Makhtesh communities, but was closer in its composition to the community of the
Central Negev Highlands (one-way ANOSIM: p < 0.002, R = 0.08) than to the
Makhtesh community (one-way ANOSIM: p < 0.002, R = 0.47) (Figure 2.4).
Figure 2.4 – The species composition of bats from the "background cluttered
space" guild, is illustrated by the proportion of each species from the total
activity in each area of the Ramon region, Israel. The three assemblages differ
significantly from each other (ANOSIM, p < 0.002).
25
2.3.2 Activity levels in the different site types
Total activity levels varied between the different site types, with the highest
total bat activity at the artificial water sources (8.57 ± 14.87 pass/hour), lower at the
natural water sources (3.67 ± 5.25), and lowest at the dry wadi sites (1.45 ± 2.89)
(Figure 2.5). Differences were significant only between the natural water sources
and the dry sites (two-tailed Kruskal-Wallis ANOVA H1,49 = 4.25, p = 0.043).
A
B
Figure 2.5 – Total activity levels for all three species (Pipistrellus kuhlii,
Eptesicus bottae and Hypsugo bodenheimeri) at different types of sites in
the three areas of the Ramon region, Israel. Letters above bars indicate
significant differences.
Kuhl’s pipistrelle’s activity levels, excluding the Makhtesh area from which it
was absent, were highest in artificial bodies of open water (4.76 ± 11.75), but were
not significantly different from the activity levels at natural water sources (1.09 ±
26
2.11) or dry wadi sites (1.34 ± 3.28). Two-tailed Kruskal-Wallis ANOVA on
transformed data: H1,51= 0.34, p = 0.89.
2.4 Discussion
2.4.1 Species composition of the "background-cluttered space" guild in the
Ramon region
The factors determining species composition at a given location can be divided
into large scale processes and local factors. The large scale processes, such as
geographical and historical phenomena, set the upper limit on species diversity,
while local factors, such as environmental characteristics and biological
interactions, can determine the site-specific species composition (Gaston 2000,
Ricklefs 2004 for all species; Ford 2005 for bats). The activity levels of all bat
species surveyed in the Ramon region followed the well-established correlation
with Ta (for instance, Williams 1961, Hayes 1997). This correlation is associated
with the seasonal pattern of activity levels that increases with the advancement of
the spring and summer, and then drops in the autumn (Korine and Pinshow 2004).
The climatic requirements of the Kuhl’s pipistrelle enable its presence in all of the
Negev (Yom-Tov and Kadmon 1998) on a large scale, but it seems to be absent
from some habitats, at least from Makhtesh Ramon as shown in Table 2.3. The
other two desert-dwelling species, Botta’s serotine and Bodenheimer’s pipistrelle,
were found in all surveyed areas. This could be due to water availability, which is
much lower in the Makhtesh, where there are no artificial water sources, and where
the hotter and dryer conditions may induce greater drinking needs than in the
northern areas of the region. In addition to the limited number of bodies of open
27
water available for the Kuhl’s pipistrelle to drink from in this region, its absence
may also be associated with interspecific competition over the use of the few bodies
of water that are available (Razgour et al. 2011). It seems that in areas that have
sufficient water available within the home range of Kuhl’s pipistrelle’s populations
their activity is not limited to the water sites alone, but they are active in dry sites as
well (Figure 2.5). This is an important observation since it may indicate that water
sources that can support Kuhl’s pipistrelle populations in dry habitats may become
stepping stones for range expansion of the Kuhl’s pipistrelle to surrounding dry
sites as well.
The choice of sites for this survey was far from optimal. The scarcity of bodies
of open water in the study area forced me to compare sites, without an effective
method to control for important factors, such as the isolation of each site, its
distance from roosts, or the flight paths that may be of more importance than actual
aerial distance. For example, the Hemet site is closer to the two Mitzpe Ramon sites
than to any Central Negev Highlands site, but it is drained by Wadi Nitzana that
shares its drainage basin with the two Mitzpe Ramon sites. Since it is the site with
the highest activity in the Mitzpe Ramon area, changing its classification would
affect the analysis. Unexpected disturbances to ponds (for example: several dry outs
of the troughs) and to equipment (for example: a bat recorder was vandalized at the
Zin site causing data loss and the changing of the site location), resulted in a
reduced sample size and some questionable reliability of some data points. The
results are also limited by the small number of ponds - just one of a type for each
area.
28
2.4.2 Range expansion of Kuhl’s pipistrelle in the Ramon region
With caution, I assume that, at least at the time of the study, Kuhl’s pipistrelle
had not yet established populations in Makhtesh Ramon. This may change in the
future. The phenomenon of time lag between the introduction of an invasive species
and the time of population outburst has been documented for many organisms,
including several vertebrates, and was explained by either changes in the
environment or genetic adaptations to the new environment (reviewed by
Simberloff 2010). The presence of a permanent body of water (NPA trough) and
development plans for visitor facilities in Makhtesh Ramon, which include an
artificial lake (NPA project manager, personal communication), may be enough to
allow Kuhl’s pipistrelle to further expand its range into areas from which it is yet
absent in the Negev. This threat is supported by the limited data collected from the
trough I set in the Alpaca Farm. The trough was monitored irregularly for bat
activity during the three years of its existence, and Kuhl’s pipistrelle activity was
apparently higher each succeeding year.
Another type of disturbance that is associated with anthropogenic development
and that gives a competitive advantage to Kuhl’s pipistrelle over desert-dwelling
bats is artificial light. Kuhl’s pipistrelles forage near street lamps while the Botta’s
serotine avoids the light (Polak et al. 2011). The Negev has been undergoing
intensive development over the past decades and more development is planned for
the coming years (Avigdor 2004). Anthropogenic development of the Negev, as
manifested by water developments and artificial illumination, provides at least two
known benefits to Kuhl’s pipistrelles. This process may support the establishment
of Kuhl’s pipistrelle populations around settlements and even in rural areas, and
29
may be causing increased competition among local desert-dwelling bat
communities (Razgour et al 2011), sharing similar ecological requirements
(Feldman et al. 2000, Korine and Pinshow 2004) .The abundance of Kuhl’s
pipistrelle in all of Israel’s climatic areas enables this species to expand its range to
all habitats, opposed to the rest of its guild that are more limited in their distribution
(Yom-Tov and Kadmon 1998). I assume that not much can be done on the regional
scale to prevent the competition of invading Kuhl’s pipistrelle with desert-dwelling
species, and the knowledge acquired on the importance of pond characteristics in
shaping the local species composition (Razgour et al. 2010), encouraged me expand
my research to identify possible management schemes that will limit the
distribution of Kuhl’s pipistrelle. Such an approach is described in Chapter Three.
30
3 Chapter Three – Managing bat communities' species composition by placing
obstructions to hamper Kuhl’s pipistrelle’s ability to drink from desert ponds
3.1 Introduction
3.1.1 Management of invasive bat species
Bat conservation is traditionally concerned with the protection of endangered
bat species by protecting either their roosting sites by placing gates at the entrance
of caves to prevent cave activities during the breeding or hibernation periods
(Martin et al. 2000), preventing habitat loss (Russo and Jones 2003), or by
conserving major foraging habitats (Sparks et al. 2005). Several bat conservation
plans have considered both roosting and foraging habitat protection (Schmidt 2003,
Ellison et al. 2003, Wermundsen 2010). Alien invasive species are considered a
major threat to biodiversity (Simberloff 2010), and bat species are threatened by
invasive terrestrial mammals such as rats (McClelland 2002). Almost all
conservation research has focused on the threats to bat species and their protection
needs. However, as diverse and abundant as they are worldwide, no insectivorous
bat has ever been declared an invasive species. This is mainly because, as opposed
to other vertebrates that humans tend to deliberately relocate (pets etc.), bats lack
such a relationship with humans in most cultures and are not deliberately
transported (Clout and Russell 2008). This might explain the absence of literature
regarding the management of invasive bat populations.
There are a few exceptions of studied cases of bats endangering other bat
species (Baagøe 1986, Arlettaz et al. 2000). In these cases, the population growth or
range expansion of the threatening populations were due to their use of artificial
31
lights for foraging, thus obtaining a competitive advantage over bats that did not
benefit from this disturbance. The same phenomenon was observed by Polak et al.
(2011) studying Kuhl’s pipistrelle in the Negev Desert. Both Arlettaz et al. (2000)
and Polak et al. (2011) suggested the control of light pollution and habitat
preservation as management tools. However, these studies did not deal with the
competitive effect of the threatening species beyond the disturbed areas. Kuhl’s
pipistrelle may pose a threat to local species beyond the surroundings of bodies of
water (Section 2.4) and therefore local bat communities may benefit from
management of Kuhl’s pipistrelle as an invasive species. Due to the lack of studies
on invasive species of bats, I explored the literature on invasive vertebrates and
birds, in particular.
The most effective approach when confronting the dangers of invasive species
is prevention -- either of the introduction itself or of further range expansion
(Wittenberg and Cock 2001, Simberloff 2010). Once an invasive species has been
established, and especially one with high maneuverability such as flying vertebrates
that may be impossible to keep away, constant monitoring and effective
management may still be useful in reducing the invader’s impact on local
ecosystems (Wittenberg and Cock 2001, Simberloff 2010). Any form of
management must take into account the species’ effect on other species in the
habitat and the interspecific interactions with other endangered species (Gumm et
al. 2011). The hierarchy of management tools suggested both by Wittenberg and
Cock (2001) and Simberloff (2010) starts with the eradication of the invader as the
most effective tool, when possible. The eradication of large scattered populations of
flying vertebrates is not easily carried out. In Europe for example, international
32
efforts for over 20 years to eradicate the American Ruddy duck (Oxyura
jamaicensis) that poses a threat to local duck species in several European countries,
are unsuccessful (Genovesi 2005). I found only one documented case of successful
bird eradication, on private farm land in Nevada Starlings (Sturnus vulgaris) had
competitively excluded local birds, and with their removal, the local bird
community has restored itself naturally (Weitzel 1988). Containment of the
invasion in a well-defined territory or exclusion from vulnerable habitats have been
discussed mostly in regard to slow growing or slow moving organisms (Brown and
Carter 1998) and are not feasible tools for flying vertebrates (Tidemann 2001).
When none of the above methods of controlling the population size and range of the
invader are feasible, mitigation has been used. Mitigation focuses on the native
species and involves taking measures to reduce the effect of the invader on native
endangered species, rather than confronting the invading species population directly
(Wittenberg and Cock 2001). In some cases, as with the common myna
(Acridotheres tristis) in Australia (Tidemann 2001), and with the protection of sea
birds (Wilcox and Donlan 2007), means of population control were used as a
successful type of mitigation. This type of management often involves a
development of artificial roosting or feeding sites for local species when threatened
by feeding competition or habitat degradation. Mitigation by the construction of
artificial roosting sites is a common practice in bat conservation, but in the context
of habitat loss and not interspecific competition (Appleton 2003, Briggs 2004).
Management practices designed to keep only specific animals away are found in the
form of fences (Andrew et al. 1997, Larsen et al. 2011) but are irrelevant for bats.
33
The activity of Kuhl’s pipistrelle is repeatedly found to be at higher levels than
any other bat species in the Negev (Korine and Pinshow 2004, Razgour et al 2010,
current survey figure 2.4), suggesting that it may be the most abundant
insectivorous bat in the region. Moreover, Kuhl’s pipistrelle is the only bat species
in the Negev that is assumed to have increased its population size over the past
decade (2000-2010) (Shalmon 2010, Korine unpublished data 2011). If the species
richness of Negev bats is to be conserved, the increasing competitive load presented
by populations of Kuhl’s pipistrelle on the rest of the desert-dwelling bat
community (Polak et al. 2011, Razgour et al 2011) requires management. Since
direct reduction of the competitive load of Kuhl’s pipistrelle by eradication or
population control methods are hardly possible, mitigation can be used to locally
reduce Kuhl’s pipistrelle activity and provide local ìcompetition freeî sites for
desert-dwelling bats.
3.1.2 Interspecific differences in the use of bodies of water as the key for the
management of desert bat communities
All four species of the “background-cluttered spaceî guild -- Kuhl's pipistrelle,
Ruppell's pipistrelle, Bodenheimer's pipistrelle, and Botta's serotine-- share the
same families of insects in their diet (Feldman et al. 2000) and foraging behavior
(Korine and Pinshow 2004). Considering that Kuhl’s pipistrelle in the Negev is an
invasive species, it seems as if any attempt at eradication or population control will
necessarily harm the endangered desert-dwelling bats. One possible mitigation
scheme may therefore lie within their different drinking behaviors, which may
influence local species assemblages.
34
Bats worldwide have been found to leave day roosts after sunset and commute
to productive foraging sites, peaking their activity levels within the first hours after
sunset and then again near dusk (Hayes 1997, Nicholls and Racey 2006). In arid
habitats, open bodies of water are preferred by bats as foraging and drinking sites
(O'Farrell and Riddle 2006, Razgour et al. 2010). For example, Myotis species in
arid habitats, were found fly shortly after sunset to nearby water holes (Adams and
Thibault 2006). The spatial distribution of foraging usually consists of commuting
from the roost to a patchy foraging site where longer amounts of time are spent and
finally returning to the same roost (Nicholls 2006). Bat species with similar diets
and morphology (body mass 4-8g) to my study species were studied in the British
Islands: the Common pipistrelle (P. pipistrellus) and the Soprano pipistrelle (P.
pygmaeus). Both species were found to commute between 0.5 and 3 km (3.8 km
max) from roosting sites to foraging areas (Nicholls and Racey 2006). The time
allocation between foraging sites or patches is determined by the resource value of
the patch, compared to the costs of obtaining the resource (Arlettaz 1996). Both
values depend on bat population density and can be influenced by competition,
promoting spatial partitioning (Kunz 1973, Arlettaz 1999, Razgour et al. 2011) and
temporal partitioning (Kunz 1973, Adams and Thibault 2006, Razgour et al. 2011)
between bat species with similar diets and foraging habitats.
Bats in the Zin Valley in the Negev Desert differ in the way they use ponds
(Razgour et al. 2010, 2011), with the Mediterranean species (the European freetailed bat and Kuhl’s pipistrelle) drinking seven and four (respectively) times more
frequently than the desert-dwelling bat species. Competition over the use of bodies
of water is found between the two sets of bats (Razgour et al. 2011): 1) The
35
Mediterranean species, the European free-tailed bat and Kuhl’s pipistrelle, compete
for drinking space over bodies of water, and seem to be obliged to drink. 2) Within
the “background-cluttered space” guild, Kuhl’s pipistrelle, Bodenheimer’s
pipistrelle and Rueppell’s pipistrelle compete for foraging space over bodies of
water. This competition results in spatial partitioning between the Kuhl’s pipistrelle,
which is associated with small temporary ponds, and the European free-tailed bat,
which is associated with large permanent ponds and tends not to visit medium and
small temporary ponds. These two species are temporally partitioned, with their
activity level speaking at different times. Similar partitioning was found among the
“background cluttered space” species that compete for foraging space. Rueppell’s
pipistrelle was found to be associated with medium ponds and its activity peaks in
the fifth and sixth hours of the night. Bodenheimer’s pipistrelle is associated with
large permanent ponds and its activity peaks during the first and last hours of the
nightand Kuhl’s pipistrelle prefers small temporary ponds and its activity peaks
between the second and fourth hours of the night. Razgour et al. (2011) suggested
that these partitioning mechanisms may prevent the expected competition due to the
high niche overlap between the two sets of competing bat species.
The Mediterranean species drink more frequently than the desert-dwelling
species, and therefore, the Kuhl’s pipistrelle's competitive load may be higher in
foraging sites that allow drinking. Several studies have reported reduced drinking
activity when the surface area of the water body was reduced in size experimentally
(Tuttle et al. 2006, Razgour et al. 2010), or when the swoop zone was limited
(Tuttle et al. 2006). Nonetheless, in both studies, the manipulations caused an
increase in the total activity at the sites, possibly due to repeated unsuccessful
36
drinking attempts. The different drinking frequencies of Mediterranean and desertdwelling bats, reported by Razgour et al. (2010), may suggest that different species
are affected more than others by such manipulations of drinking area. Tuttle et al.
(2006) do not differentiate between the responses of different species to the
manipulation, but Razgour et al. (2010) do. They found that the manipulation,
leaving 8 m of pond free for drinking, reduced the activity of all four species of the
ìbackground-cluttered spaceî guild. These results may have been due to the short
and intensive periods of disturbance caused by the manipulation. The results do not
shed light on the question of whether a stronger manipulation, preventing Kuhl’s
pipistrelle from drinking, would have a stronger effect on Mediterranean species.
My experimental approach was an attempt to show whether such a disturbance can
prevent Kuhl’s pipistrelle from drinking, thus reducing competitive loads from the
desert-dwelling species, which will benefit from a higher value foraging site.
I hypothesized that placing obstructions above open bodies of water would
hamper the drinking ability of Kuhl’s pipistrelle and would have a lesser effect on
desert-dwelling bat species since the former drink more frequently than the latter.
The resulting reduction in Kuhl’s pipistrelle activity would create "competition
free" foraging sites for desert-dwelling bats.
I did three different field experiments and tested the following predictions:
1) Increasing the density of obstructions over a body of water, used only by
Kuhl’s pipistrelle and only for drinking, reduces the drinking frequency of the bats
and, eventually, prevents it.
37
2) The activity level of Kuhl’s pipistrelle (measured by their echolocation
calls) is higher in un-manipulated ponds (explained hereinafter) than in the same
ponds, once manipulated. The activity level of Ruppell’s pipistrelle,
Bodenheimer’s pipistrelle and Botta’s serotine is higher in manipulated ponds
(explained hereinafter) than in the same un-manipulated ponds due to reduced
competition from Kuhl’s pipistrelle. Field experiment II (manipulation of natural
ponds in the Zin valley (Section 3.2.2)), and the following year field experiment
III (manipulation of isolated natural ponds (Section 3.2.3)) were designed to test
this prediction.
The manipulation was formed by obstructions constructed over open bodies of
water to hamper bat drinking, as is explained in detail (Section 3.2.1).
3.2 Methods
3.2.1 Field experiment I: Manipulation of the swimming pool
Study area and site
This experiment took place in Midreshet Ben Gurion in the Negev Desert, in the
summer of 2010. In this desert region rain occurs during the winter and averages 97
mm per year. Ta are highest during summer and are lowest in winter, with a daily
mean of 25.3 ºC in August, and 9.7 ºC in January in Midreshet Ben-Gurion
(Meteorology unit BIDR 2010). The study site used was the local swimming pool,
25 m by 25 m and ‘L’ shaped (Figure 3.1), located at 30°51'13.57"N, 34°47'08.53"E
and at 478 m elevation. This pool was chosen since Kuhl’s pipistrelle had
previously been observed drinking in it and it is located ~ 100 m from a known
Kuhl’s pipistrelle roosting site (Berger-Tal et al. 2008). Kuhl’s pipistrelle is
38
apparently the only species that uses this site (Korine, personal communication, and
verified by vocalizations recordings during the experiment).
Experimental design
The swimming pool was covered with a grid of black Polypropylene string with
an average diameter of 2 mm, limiting the water surface to sections of 1  1 m. This
was done to prevent the Kuhl’s pipistrelle from drinking from the pool. The
experimental plot was created by leaving the non-experimental area covered by the
string grid and uncovering a 9  9 m experimental area (Figure 3.1). Four different
treatments were done on the 9  9 m section of the pool. For the control treatment,
the experimental area was left uncovered, and for the other treatments, this area was
sectioned into varying sized squares: 4.5  4.5 m, 3  3 m and 1  1 m (Figure 3.1).
The string was elevated 10 cm above the surface of the water.
25m
Figure 3.1 A diagram of the
swimming pool, at which the
experiment was carried out, is
shown. It measured 25 m in length
and 12.5 m in width. The black line
represents the 1  1 m fixed grid
covering the non-experimental area.
The area without a black line
represents the 9  9 m experimental
area (also used as the 9  9 m control
treatments). The other colored lines,
green (1  1 m), red (3  3 m) and
1m
blue (4.5  4.5 m) represent the three
different treatments.
3m
4.5 m
12.5m
39
The four treatments were scheduled to be done at different times over five
evenings, to control for the fact that bat activity varied at different times throughout
the night. This also controlled for possible affects on drinking due to a preceding
treatment, as each treatment was preceded by a different treatment on each of the
nights. The experiment began each night 30 min after sunset (~19:30), and the
periods used for the different treatments each night were: 20:10 - 20:30, 21:30 21:50, 22:10 - 22:30 and 22:40 - 23:00.
I counted the number of passes and drinking events over the experimental area
in a set period of time. This was done by direct un-aided observations. In all of the
trials, there was one artificial light source, set 10 m away from the pool, and
observers used head lamps. I used an AnaBat detector to monitor the experimental
area acoustically. This allowed an auditory prompt for bat arrival, and the data
recorded were analyzed using AnaLookW (3.3) software to ascertain that all
observations were of Kuhl’s pipistrelle.
Data analysis
Since the data on the number of drinking events were not normally distributed,
their variance among treatments lacked homogeneity and since many ‘0’ values
were recorded, some of the statistical tests required transforming the activity data
by log(x+1). A repeated-measures ANOVA was used to determine whether there
was a difference between nights. When the different nights were found to have no
effect on bat activity, a one-way ANOVA was used to determine whether there was
a difference between treatments. All tests done for all three field experiments were
two-tailed, and the results were considered to be significant at p < 0.05. All tests in
the three field experiments were done using STATISTICA 7.
40
3.2.2 Field experiment II: Manipulation of natural ponds in the Zin Valley
Study area and sites
This field experiment examined drinking ability of bats from manipulated ponds
in areas where Mediterranean bat species are well established – the Zin Valley in
the proximity of Midreshet Ben-Gurion (30º52' N, 34º47' E) in the Negev Desert
Highlands (Climatic description in section 3.2.1). The field experiment took place
in temporary and permanent open ponds located in the Zin and Akkev Wadis. In
both wadis, springs sustain permanent ponds all year round, while temporary ponds
dry out during the spring or the beginning of the summer (Table 3.1).
Table 3.1 – Sites chosen for experiment II. All sites are located within the Zin
Valley in the Negev, Israel. The measures marked by * changed during the
three week period of the experiment. The values in the table are the measured
maxima at the time of the experiment.
Site name
A.White Cliff East
B. Akkev East
C. White Plains A
D. Bor Nabati
E. White Plains B
F. White Cliff West
G. Australia Pond
H. Conglomerate Pond
J. Heart Pond
K. Salon Pond
L. Akkev Horseshoe
Description
Temporary pond
inWadi Zin
Temporary pond in the
Akkev Wadi
Temporary pond in the
Akkev Wadi
Temporary pond in the
Zin Wadi
Temporary pond in the
Akkev Wadi
Temporary pond in the
Zin Wadi
Temporary pond in the
Zin Wadi
Temporary pond in the
Zin Wadi
Temporary pond in the
Akkev Wadi
Temporary pond in the
Zin Wadi
Temporary pond in the
Akkev Wadi
Compass
Coordinates
30°50'37.69"N
34°47'24.29"E
30°49'35.38"N
34°48'38.82"E
30°49'54.71"N
34°48'46.51"E
30°50'31.50"N
34°48'42.32"E
30°49'50.54"N
34°48'46.61"E
30°50'36.53"N
34°47'22.37"E
30°50'30.24"N
34°46'37.11"E
30°50'14.24"N
34°46'30.17"E
30°49'3.59"N
34°48'45.04"E
30°50'38.82"N
34°46'59.49"E
30°49'33.13"N
34°48'35.42"E
Pond
length
(m)*
Distances
from nearest
pond(m)*
8
50
7
10
19
5
10
20
15
0
5
50
6
150
8
3
3
5
50
30
5
50
41
Figure 3.2 - Field experiment temporary pond sites in the Zin Valley.
Experimental design
From among many temporary ponds in the Zin Valley that were filled with
water by the winter floods of January 2010 (Israel Meteorology Service 2010), I
chose 11 that held water for several months. This allowed for the experiment to
begin in April when bat activity levels are sufficiently high. I chose ponds that were
large (mean pond length: 7.67±4.96 m) and deep enough (>15 cm), so I could
expect them not to dry out during the three weeks of the experiment, and that were
at least 3 m long to ensure that they would facilitate drinking activity and not only
foraging. The ponds were not isolated (mean distance from nearest other pond:
47.5±51.67 m, min=0 m, max=150 m), but were chosen to make distances between
ponds as far as possible, to prevent calls from a nearby pond from being mistakenly
accounted for in the analysis. The experiment was done in three ponds
simultaneously, but I manipulated only one pond at a time (Table 3.1). This was
42
done to control for temporal factors that may affect bat activity. I did the
experiment from the beginning of April to the end of July 2010.
I recorded bats by placing an AnaBat detector 3-5 m from the pond bank. Since
experimental treatments required several nights of monitoring, AnaBat detectors
were concealed in hard plastic boxes with their microphones protruding, facing 45°
vertically toward the pond. The devices were connected to a 12 v battery, allowing
for continuous monitoring for seven nights. Proximate Ta was measured for each
recording night and for each pond using iButton® data loggers as described in
Section 2.2.3. I measured pond length and the distance from the nearest open body
of water with a tape measure (distances < 30 m), and by locating sites on a map
aided by hand held G.P.S (eTrexÆ-H by Garmin, accuracy ±25m) and measuring
the line of site, for longer distances.
Each experiment consisted of three phases: 1) Recording of bat activity levels
for seven nights before the manipulation (control treatment); 2) manipulation of the
size of the pond (Figure 3.3), and recording bat activity for seven nights; and 3)
recording for seven nights after removing the manipulation (control treatment).
Table 3.2- Temporally staggered use of ponds for field experiment in the Zin Valley,
Israel. Each pond was monitored for bat activity with three following treatments. In
most of the experiments, three ponds were handled simultaneously, but never with the
same treatment in two ponds at the same time, to control for the effect of
environmental factors
Week
number
Pond 1
Pond 2
Pond 3
Pond 4
Pond 5...
1
2
Control Manipulation
Control
3
4
5
6
Control
Manipulation
Control
Control
Manipulation
Control
Control
Manipulation Control
Control Manipulation
43
The obstruction of the ìswoop zoneî was created by a network of corrugated
plastic sheets, leaving the total surface area of the pond unchanged, but minimizing
the largest free water surface to 1 × 1 m (Figure 3.3).
Figure 3.3 – An example of
the network made of
corrugated plastic sheeting,
to cover the pond surface.
This is the pond in the
Alpaca farm near Mitzpe
Ramon, Israel.
3.5 m
2m
Data Analysis
I counted and normalized the bat calls as described previously (section 2.2.4).
Following Ciechanowski (2002), I used the proportion of Kuhl’s pipistrelle’s
activity level from the total bat activity within the "background-cluttered space"
guild, and I used arcsine transformation on the proportions to increase the
sensitivity of the index at extremely high and low proportions.
The transformed data were not normally distributed. To test if the manipulation
affected the proportions, I performed a non-parametric Kruskal-Wallis ANOVA,
with the proportion of Kuhl’s pipistrelle activity as the dependent variable, and for
three treatments (control 1, manipulation, post manipulation). The effects of other
factors, such as Ta, pond length and distance from nearest pond -- on the proportion
of Kuhl’s pipistrelle activity were tested using a Spearman rank correlation.
44
Another statistical approach was to look for effects of the manipulation between
the different nights of each treatment (rather than just between treatments). This
was done by calculating linier regression slopes of the proportion of Kuhl’s
pipistrelle activity between the nights of each treatment in each pond. Then I used
the regression slopes of the different treatments as the dependent variable to test for
changes in species composition during treatments. By this approach positive values
of the slops would mean that Kuhl’s pipistrelle activity increased compared to the
activity of desert dweling species, while negative values would indicate that it has
decreased during the treatment.
3.2.3 Field experiment III: Manipulation of isolated natural ponds
Study area and sites
The experiment was conducted in eight bodies of water in a wide variety of
habitats in the Negev Highlands and the Dead Sea area. The sites were chosen for
their isolation from other potential drinking sites (mean distance of site from the
next nearest open body of water: 1650 ± 840 m, max: pond no.4 = 3000 m, min:
pond no.1 = 300 m) in order to ensure that bats lacked the option of drinking at a
nearby pond during the manipulation treatments (Table 3.3). All ponds were large
enough to ensure that bats could drink but small enough to be manipulated easily
with the string grid (mean length: 7.28 ± 2.69 m, min: pool no.6 = 4 m, max: pool
no.1 = 20 m).
45
Table 3.3 – Sites chosen for experiment III. All the sites were comparatively isolated
from other bodies of water that could serve as other potential drinking sites for bats (=
length of pond > 3m). The measures marked by * may change over time and are here
mentioned as recorded at the time of the experiment.
Site name
1. Revivim
2. Makhtesh
Gadol
3. Ein
Yorkeam
4. Gev Yamin
5. Ein UmTina
6. Gev Zarhan
7. Serpentine
Pond
8. Ein Ahava
Description
Temporary pond in
Revivim Wadi by the
road (40) side
Temporary pond at
the exit of the
Makhtesh
Permanent spring
and pond
Temporary pond in
Yamin Wadi
Temporary pond in
Zarhan Wadi
Temporary pond in
Zarhan Wadi
Temporary pond in
Zin Valley near EinAvdat National Park
Permanent spring
and pond in the Dead
Sea Valley
GPS Coordinates
Pond
length(m)*
Distance from nearest
body of water(m)*
31° 0'34.31"N
34°46'44.98"E
20
300
30°57'2.03"N
35° 1'48.20"E
6
1800
12
1800
7
3000
5
2100
4
2100
30°50'35.51"N
34°46'44.84"E
9
1300
30°57'21.92"N
35°21'50.02"E
8
800
30°56'13.28"N
35° 2'30.57"E
30°56'38.19"N
35° 4'22.74"E
30°49'9.97"N
34°56'36.99"E
30°50'1.04"N
34°57'29.48"E
20 Km
Figure 3.4 - Field experiment sites in isolated ponds in various parts of the Negev.
46
Experimental design
I tested the effect of the manipulation on a shorter temporal scale then In field
experiment II, with two treatments, ‘Manipulation’ and ‘Control’, which were
alternated every 20 min. I selected this time because I demonstrated in the pool
experiment that it was sufficient in which to observe behavioral differences in
Kuhl’s pipistrelle (Section 3.3.1). Each experiment ran for two nights, switching
treatment orders to control for the effect of time, since drinking activity was
observed to peak at beginning of the night (Table 3.4).
Assembly of the manipulation construction was done in day light, and
recordings and the first treatment began 20 minutes after sunset and ended after four
treatments, or continued if activity was still high. Recording was done with AnaBat
detectors, and a proximate for Ta was measured with iButton® data loggers as
described (Section 2.2.3).
I measured the length of each pond with tape measure, and the distance from the
nearest water source was measured by identifying the ponds on a 1:50,000
topographical map and measuring the line of site. For the manipulation, I
constructed, for each pond, a special grid from black Polypropylene string (average
diameter 2 mm) on a frame, in the shape of the pond surface, made of metal wire.
This design made alternating between treatments fast, taking less than one minute in
most cases.
47
Table 3.4 -Design of experiment III: Studying manipulation effects on bat activity
at isolated natural ponds in the Negev, Israel. This experiment was based on
alternating the treatments several times (4-6 treatments per night), two nights in
each site, and starting with a different treatment each night. For full list of ponds
see Table 3.3.
Treatment
number
Start time
from to
Pond 1,
1st night
Pond 1,
2nd night
Pond 1,
1st night
Pond 1,
2nd night
Ponds
3…6
1
3
4
5
6
20min
40min
60min
80min
100min
Control
Manipulation
Control
Manipulation
Manipulation
Control
Manipulation
Control
Manipulation Control
Manipulation
Control
Manipulation
Control
Manipulation Control
Control
Manipulation
Control
Manipulation
0min
2
Control Manipulation
Control Manipulation
Data Analysis
I counted and normalized the bat calls as described previously (Section 2.2.4),
dividing each treatment into four sections of five min each. When analysis required
the use of the activity levels of the full 20 min. of treatment, I used the mean of the
four samples to avoid pseudo replication. To identify changes in species
composition, I used the proportion of Kuhl’s pipistrelle activity as described above
(Section 3.2.2).
The effect of the manipulation on the proportion of Kuhl’s pipistrelle within the
bat communities of the different sites was tested by a general linear model in which
the proportion of Kuhl’s pipistrelle activity was the dependent variable. The
treatment and the site (random) were used as categorical factors, and the treatment
48
number (first each night = 1, 2nd = 2, etc.) and proximate Ta were used as
continuous predictors. I also looked for effects during the treatment using
regression slopes of the treatment sub-units (Section 3.2.2).
3.3 Field experiment results
3.3.1 Manipulation of the swimming pool
In total, I obtained 170 observations of bat activity at the swimming pool during
five nights, made up of 152 flight events and 18 drinking events. All recorded
observations were identified as Kuhl’s pipistrelle.
No significant difference in activity levels or in drinking frequency were found
among the different nights of the experiment (repeated-measures ANOVA, F3 =
0.645, p = 0.605). Therefore, data from all nights were pooled for the rest of the
analysis. Drinking passes, as a proportion of total activity, was significantly
different between treatments (one-way ANOVA: F3,19 = 3.926, p = 0.028). The
highest proportion of drinking events to total activity was recorded in the control
treatment, and no drinking events were recorded in the 1  1 m and 3  3 m
treatments.
49
70
Passes
without
drinking
passes per tretment
60
50
Drinking
passes
40
30
20
10
0
9mx9m
4.5 m x 4.5 m
3mx3m
Treatment
1mx1m
Figure 3.5 – Passes without drinking and drinking passes of Pipistrellus kuhlii in
the swimming pool experiment during the different treatments. Each treatment
divided the experimental plot into sections of different size: 1  1 m, 3  3 m, 4.5 
4.5 m, and 9  9 m (control). The proportion of drinking from the total activity, was
significantly different between treatments (one-way ANOVA: F3,19 = 3.926, p =
0.028).
3.3.2 Manipulation of natural ponds in the Zin Valley
Out of the 11 ponds that I chose, useful data were obtained from eight (Table
3.6). I did not use the data from three of the ponds for the following reasons: one
pond dried out during the manipulation treatment (Pond E), and there were
technical malfunctions at ponds H and L.
Total bat activity and species composition at the experiment sites
Total bat activity varied significantly between ponds (Kruskal-Wallis ANOVA:
H6,144 = 3.17, p < 0.0001) but did not vary between the different nights (Kruskal-
50
Wallis ANOVA: H93,144 = 87.07, p = 0.653) (Table 3.6). Total bat activity was not
correlated with Ta (Spearman rank correlation: R105 = 0.083, p = 0.399).
Kuhl’s pipistrelle activity as a proportion of total activity, was not significantly
different among the ponds (Kruskal-Wallis ANOVA: H6,143 =14.145, p=0.28).
Kuhl’s pipistrelle dominated all ponds with average proportion of 0.957±0.074
from the total bat activity. The proportion of Kuhl’s pipistrelle activity was
positively correlated with pond length (Spearman rank correlation: R142 = 0.273,
p = 0.001).
Manipulation effects on species composition
The manipulation did not reduce the proportion, of Kuhl’s pipistrelle activity of
total bat activity. Proportional activity of Kuhl’s pipistrelle was not affected by the
treatments (Kruskal-Wallis ANOVA: H2,143 = 0.3427462, p = 0.8425) . The
treatments did not account for any significant differences in the activity levels of
Kuhl’s pipistrelle (Kruskal-Wallis ANOVA: H2,143 = 3.402, p = 0.1825), the activity
levels of desert-dwelling bats (Kruskal-Wallis ANOVA: H2,70=0.214, p=0.898), or
total bat activity (Kruskal-Wallis ANOVA: H2,144 = 2.638435, p = 0.2673). The
regression slopes of the proportions of Kuhl’s pipistrelle between the nights did not
differ between treatments (one-way ANOVA: F2 = 1.73, p = 0.201), and the slope
of the regression between the night of manipulation treatment was negative in some
ponds but positive in others (Table 3.7), indicating that there was no consistent
effect of the manipulation on any of the species activity levels between the
treatment nights. The slopes were not affected by pool length or distance to the
nearest pond.
51
Table 3.6 – Total bat activity and proportional activity of Kuhl’s pipistrelle for each night for the
eight ponds from which data were obtained in experiment II in the Zin Valley, Israel.
P. kuhlii activity
(passes per night)
Total bat activity
(passes per night)
432.9±448.1
470.4±485.5
P.kuhlii passes / total
passes
0.96±0.03
27.6±12.8
38.0±16.8
0.98±0.03
C. White Plains A
140.8±116.1
154.1±124.9
0.94±0.08
D. Bor Nabati
126.6±109.4
135.5±113.3
0.94±0.10
F. White Cliff West
40.1±44.1
39.4±45.4
0.97±0.05
G. Australia Pond
83.2±55.0
95.5±61.5
0.97±0.03
J. Heart Pond
439.9±598.8
444.4±598.8
0.99±0.05
K. Salon Pond
34.9±39.5
39.0±41.8
0.91±0.12
164.6±318.8
173.1±324.2
0.96±0.07
Site name
A.White Cliff East
B. Akkev East
Total
Table 3.7 – The linier regression slopes of the proportions of Pipistrellus kuhlii of
total bat activity between the nights of each treatment of field experiment II in the Zin
Valley, Israel. Positive slops indicate an increase in the proportion of P. kuhlii of total
bat activity during the treatment, and negative slopes indicate a decrease. The type of
treatment had no significant effect on the slopes.
Site name
Control
Manipulation
Post Manipulation
A.White Cliff East
0.17
-0.06
0.03
B. Akkev East
0.17
0.04
0
C. White Plains A
0.39
-0.03
-0.03
D. Bor Nabati
0.10
0.03
-0.03
F. White Cliff West
0.07
0.03
0.39
G. Australia Pond
-0.03
-0.02
-0.02
J. Heart Pond
0.03
0
-0.02
K. Salon Pond
-0.10
0.10
-0.08
52
3.3.3 Manipulation of isolated natural ponds
Data were obtained from six out of eight ponds (Table 3.8), with two ponds
lacking sufficient activity of the appropriate species for the analysis (ponds 5,6).
Total bat activity and species composition at the experiment sites
Total bat activity levels differed significantly at the six ponds (GLM: F1,43 =
6.586, p = 0.0001) and so did the proportion of Kuhl’s pipistrelle activity of total
bat activity (GLM: F5,35 = 5.22, p = 0.016) (Figure 3.6). Activity levels were
positively correlated with Ta for each pond (GLM: F5 = 6.562, p = 0.0001). The
proportion of Kuhl’s pipistrelle activity at each site was negatively correlated with
Ta at the site (GLM: F1,35 = 12.72, p = 0.001).
Table 3.8 – Activity of Pipistrellus kuhlii and total bat activity in the eight
ponds used for the experiment. Ponds no.5 and 6 were excluded from the
analysis due to low / absent activity of P. kuhlii.
Site name
P. kuhlii activity (passes
per treatment)
152.56±81.00
Total bat activity
(passes per treatment)
174.94±97.38
P.kuhlii passes / total
passes
0.85±0.24
2. Makhtesh
Gadol
3. Ein Yorkeam
16.00±22.85
51.19±56.87
0.35±0.27
21.61±41.57
83.00±78.60
0.40±0.42
4. Gev Yamin
32.33±36.58
61.5±60.38
0.55±0.26
5. Ein Um-Tina
1.33±0.66
1.33±0.66
1
6. Gev Zarhan
0
2.05±2.49
0
7. Serpentine
22.33±20.69
26.96±26.70
0.93±0.16
8. Ein Ahava
2.88±4.57
92.88±40.39
0.03±0.05
41.28±34.54
81.74±60.06
0.52±0.23
1. Revivim
Total (analyzed
ponds only)
53
Figure 3.6 – The proportions of Pipistrellus kuhlii activity levels and
desert-dwelling bats (Eptesicus bottae and Hypsugo bodenheimeri) of the
total activity in each of the sites used for the experiment III in isolated
ponds in the Negev, Israel. Proportions of P. kuhlii of the total bat activity
were found to be significantly different (GLM: F5,35 = 5.22, p = 0.016).
Manipulation effects on species composition
The manipulations had no significant effect on the proportion of Kuhl’s pipistrelle
activity of the total bat activity when all six ponds were included in theanalysis (GLM:
F(6,35)=1.02, p=0.429). When I included only the three sites that had higher proportions of
Kuhl’s pipistrelle activity to begin with (Ponds 1, 4 and 7. Table 3.8), the proportion of
Kuhl’s pipistrelle activity was significantly lower in the manipulation treatments (GLM:
F(2,11)=4.6, p=0.035) (Figure 3.7).
54
*
- -
Figure 3.7 – The proportion of Pipistrellus Kuhlii activity of total bat activity in the
different treatments at each site. P. Kuhlii proportional activity was significantly lower
during manipulation treatments only when sites marked by asterisk (*) were included.
When testing the different factors using the linier regression slopes of the
proportions of Kuhl’s pipistrelle activity within treatments as the dependent
variable, trends were similar to those of proportions were observed: treatment
slopes were significantly affected by site (GLM: F5,34=6.89, p = 0.0004), and were
positively correlated with the treatment from the beginning of the night (GLM:
F5,34=10.44, p = 0.003). The regression slopes were not significantly reduced by the
manipulation (GLM: F6,34 = 0.17, p = 0.98). Linear regression slopes of proportions
of Kuhl’s pipistrelle activity were also not affected by pool length or distance to
nearest pond.
55
3.4 Discussion
3.4.1 Manipulation of the swimming pool
The size of clear space above the water was found to effect the drinking activity
of Kuhl’s pipistrelle. In accord with my prediction, increasing the density of the
string above the water caused a decrease in the number of drinking events in
proportion to flight events, over the experimental area. This indicates that there is a
certain size of water surface area that must be unobstructed to allow drinking by
Kuhl’s pipistrelle. This is consistent with previous studies (Razgour et al 2010,
Tuttle et al., 2006, Jackrel and Matlack 2010). The fact that total bat activity did not
drop with the increase of string densities, along with drinking activity, may be due
to bat approaches towards the pond in attempts to drink, and flying off once the
disturbance was detected. A similar phenomenon of increase in bat activity when
drinking was disturbed was observed by Tuttle et al. (2006) and by Razgour et al.
(2010).
No drinks occurred in the 3  3 m treatment or the 1  1 m treatments, but
drinking did take place in the 4.5  4.5 m treatment. This suggests that the
minimum length of unobstructed water required for Kuhl’s pipistrelle to drink lies
between 3-4.5 m. However, based on my field observations, as shown in Table 2.1,
a large population of Kuhl’s pipistrelle forage around the NPA trough in Nitzana
Wadi being the only open body of water in the area. This trough, even when
enlarged for the survey, did not exceed 3  2.5 m, yet was used for drinking
(personal observation). Theoretically, the explanation for these results could be that
the obstructions, laid < 3 m apart, were dense enough to prevent the identification
56
of the body of water. This explanation, though, is challenged by Greif and Siemers
(2010) who reported that the innate recognition by echolocation is a stronger cue for
water recognition than prior knowledge of the nature of water bodies by bats.
Another problem with this explanation is that the Kuhl’s pipistrelle’s roost close by
(Berger-Tal et al. 2008) and are assumed to have prior knowledge of the pool as a
drinking source. Another way to look at the experimental results, not as indicating a
physical limit of 3  3 m prohibiting drinking altogether, but rather as an indication
of the bats’ immediate response to the manipulation, which may weaken with time.
Previous studies by Razgour et al. (2010) do not shed light on this question since
the length of clear water area after the manipulation were much larger (>8m).
However, Tuttle et al. (2006) and Jackral and Matlack (2010) did reduce clear water
surface in troughs to less than 2 m and still observed drinking by several bat
species. This contradiction could be resolved by using a similar experimental design
over an extended time period to determine whether Kuhl’s pipistrelle would remain
present in the area and resume drinking at least in the 3  3 m plots, or would
change their foraging and drinking behavior and start drinking elsewhere.
Despite these remaining questions, it seems safe to assume that in I have found
a method that does prevent the Kuhl’s pipistrelle from drinking, for a short time
frame, by making a grid of 1 x 1 m, and this was the method used in the field
experiments, as described (Section 3.2), to manipulate natural ponds used by Kuhl’s
pipistrelle and other bats as drinking and foraging sites.
57
3.4.2 Manipulation of natural ponds in the Zin Valley
The experiment in the Zin Valley was intended to explore the possibility of
manipulating species' composition by disturbing the drinking ability of the Kuhl’s
pipistrelle, that is known to drink often. Though activity levels varied between sites,
species composition was similar (Section 3.3.2). My manipulations did not affect
the activity levels of any bat species, and I offer two explanations for the failure of
this experimental design. First, my indicator of changes in species compositions
was measuring activity levels of bats without the ability to distinguish between
drinking and foraging flights. Previous studies that manipulated ponds found
reduced drinking flights but an increase in total activity (Tuttle et al. 2006, Razgour
2010). The increase in total activity may have occurred during my manipulation
treatments, and interpreted in the results as “No reduction of activity” even when it
did decrease. Second, the local conditions of the experiment may have affected the
manipulation’s success. The Zin Valley has received extraordinary amounts of
water in the winter of 2010, mainly in a rare rain event on the 17-18th of January,
with 139mm of rain in 48 hours at Midreshet Ben Gurion (Israel Meteorology
Service 2010). This major rain event left the Zin Valley full of ponds in near each
other (average distance between recording site to the nearest drinking site =
47.5±51.7m) half way through July. Thus, drinking was not a limiting factor on
foraging for Kuhl’s pipistrelle at the time of the experiment. A manipulated pond
was not abandoned, presumably because drinking was available at nearby ponds.
The same explanation was suggested by Ciechanowski (2002) to explain why bats
did not avoid small ponds in the forest that were elsewhere neglected, due to those
ponds' proximity to larger ponds that allowed them to drink.
58
According to the first explanation, the total activity level remains high when
ponds are manipulated, so the idea of disturbing the Kuhl’s pipistrelle drinking
cannot be used as a management tool since it would not reduce its competitive load
on the other species of the guild. If the second explanation is correct and the
manipulation works only when the distance to the nearest drinking site is
considerable, then it would be an ideal management tool to reduce the disturbance
caused by isolated troughs. Deciding between the two explanations could be done
either by repeating the same experiment, but using a method that can separate
drinking from foraging activity, or by manipulating isolated bodies of water as I did
in experiment III.
3.4.3 Manipulation of isolated natural ponds
The important finding from this experiment lines with my original predictions;
in certain ponds and for a short period, smaller proportions of Kuhl’s pipistrelle
were observed during the manipulation by a string grid. My conclusion is that the
manipulation changed the activity levels, thus decreased the competition on the
desert-dwelling species, Bodenheimer’s pipistrelle and Botta's serotine. However,
this approach is effective for short periods and only if the ponds are isolated. These
results are different from the results of experiment II in the Zin Valley, and from
those of Razgour et al.(2010), where the pond surface was partly covered. Their
experiment was done in the same area with the same species of bats, and found that
the activity levels of all three species were reduced by the manipulation. The
different results way be due to the fact that the ponds I used in experiment II and
by Razgour et al (2010) were not isolated.
59
An alternative interpretation of Razgour et al. (2010) results may be the material
used to cover the ponds. They used a smooth, clear plastic sheet as a cover, which
was recently shown by Greif and Siemers (2011) to imitate the acoustics of the
water surface and might have been perceived by bats as regular water. Thus the
reduction of bat activity found by Razgour (2010) may have been due to the
reduction in its foraging quality caused by the prevention of water access. This may
explain why all three species were affected in Razgour et al. (2010) experiment.
In contrast to the Zin Valley measurements in experiment II, where species
composition was similar in all sites, in experiment III, the significant differences in
species composition turned out to form a gradient between the six sites in the
proportion of Kuhl’s pipistrelle activity of the total bat activity. Higher proportions
of Kuhl’s pipistrelle activity occurred in the sites with lower Ta, as would have been
expected from the species known distribution and Mediterranean origin (Yom-Tov
and Kadmon 1998). The manipulation did not have a significant effect on the
proportion of Kuhl’s pipistrelle at all the sites but during the manipulation Kuhl’s
pipistrelle proportions were smaller in the sites where Kuhl’s pipistrelle was more
abundant. This can be explained by stronger competitive load on the desertdwelling species, in sites where Kuhl’s pipistrelle dominates the bat communities.
In sites with stronger competition, the reduction of competitive load by the
manipulation was detectable.
60
4 Chapter Four – General discussion
4.1 The current distribution of Kuhl’s pipistrelle and its impact on local bat
communities
The exact process that brought about the current distribution of Kuhl’s
pipistrelle in the Negev Desert and the rate of its expansion are not clear. I,
however, suggest that anthropogenic development processes involving the
introduction of new water bodies play a role in the Kuhl’s pipistrelle range
expansion. Evidence for the role of new bodies of water in the species' range
expansion is the constant growth in the activity levels of Kuhl’s pipistrelle, which I
observed at the Alpaca Farm pool since it was built (March 2009- August 2011).
Range expansion will not end anywhere in the Negev due to climatic reasons since
Kuhl’s pipistrelle have been found as far away and in as hot a climate as Eilat
(Zelenova and Yosef 2003, Shalmon personal communication 2011). Field surveys
and observations confirm that Kuhl’s pipistrelle are not limited to anthropogenic
sites or to water sources but are active in all habitat types within the range of their
distribution (Korine and Pinshow 2004). Kuhl’s pipistrelle are apparently absent
from the eastern part of Makhtesh Ramon, and due to their high frequency of
drinking (Razgour et al 2010), it can be assumed that the bats are absent from most
of the southern Negev, i.e., from the Ramon cliff and down to the Paran Valley, that
lacks open bodies of water. The important exceptions to this lack of drinking
opportunities are the NPA troughs in Makhtesh Ramon and the Paran Valley, the
tourist lake being built in Makhtesh Ramon, and the waste water pool in the
Shdema facility (30∞30'46.78"N, 34∞56'58.10"E). To date, there have been no
61
more than anecdotal sightings of Kuhl’s pipistrelle in Makhtesh Ramon and the
Paran troughs, but my recent observations using AnaBat detectors,indicate regular
activity of Kuhl’s pipistrelle near the Shdema waste water pool. Bodies of open
water such as Shdema waste water pool should be focal points of any program
aimed at monitoring the range expansion of the Kuhl’s pipistrelle in the Negev.
4.2 The effect of pond manipulation on species composition
Sharing the same diet, using the foraging mode (flying low above the
vegetation) and preferring the micro-habitats surrounding open bodies of water,
Kuhl’s pipistrelleare in competition with the other members of their guild (Razgour
et al. 2011).The competition is over foraging space more than over drinking area
since the frequency of drinking flights in desert-dwelling species is significantly
lower compared to Kuhl’s pipistrelle (Razgour et al 2011). I claim that the presence
of Kuhl’s pipistrelle may cause competitive exclusion of the desert-dwelling
species. This may seem contradictory to Razgour’s conclusion of Kuhl’s pipistrelle
reducing their activity at preferable habitats once they are dominated by Rueppell’s
pipistrelle and Bodenheimer’s pipistrelle during the spring and fall. My claim is not
based on a different data set but on a different perspective. When using community
ecology tools and treating Kuhl’s pipistrelle as an integral part of the community,
one can calculate competitive loads, as Razgour et al. (2011) did, and conclude that
the Kuhl’s pipistrelle are subdued by Rueppell’s pipistrelle and Bodenheimer’s
pipistrelle more than vice versa. From my conservation perspective, any
competition by the range expanding species Kuhl’s pipistrelle with a local species is
a disturbance to the latter. Proceeding along this line, I view any reduction of
62
Kuhl’s pipistrelle activity in its shared habitats with desert-dwelling species as an
important part of the mitigation (Wittenberg and Cock 2001) necessary for the
conservation of the Negev bat communities.
4.3 The potential use of the grid as a management tool for the Negev bats
I have shown in the pool experiment that the drinking of Kuhl’s pipistrelle can
be limited and maybe even prevented by a string grid, at least temporarily. The grid
did not appear harmful to bats since no collisions with the strings or accidents
(falling into the water) were observed, as was also observed by Tuttle et al. (2006).
This is a low cost tool and seemingly harmless to other components of the desert
ecosystem. The field experiments did not give a conclusive answer to how does
manipulation affect the activity patterns of the different species. I found that, in
isolated ponds with high proportion of Kuhl’s pipistrelle, the short term
manipulation reduced the activity of Kuhl’s pipistrelle compared to the activity of
desert dwellers. "Isolated bodies of water" may be a specific case, relevant to only a
handful of sites in the Negev. However, these bodies of water, mostly NPA
troughs, have high potential to facilitate the further range expansion of the Kuhl’s
pipistrelle. The grid cannot be put to use as a management tool until its long-term
efficiency is studied over a period of months or years since significant effects of the
manipulation were demonstrated only in the last experiment, when treatments 20
minutes long were used. Though seemingly harmless, possible effects on other
wildlife should be looked In to as well. Even if this manipulation is proven to be
efficient on a large temporal scale, any long term use of the grid should be
accompanied by monitoring of bat activity since local micro-habitat characteristics
63
have an important effect on community composition (Razgour et al. 2010) and will
determine the outcome of the manipulation at each specific site.
4.4 Mitigation and reconciliation rather than aggressive eradications as the
future of invasive species management
Kuhl’s pipistrelle has invaded some desert habitats, yet it can hardly be treated as
a dangerous pest. On the contrary, as a widely distributed insectivorous bat, which has
a strong affiliation to anthropogenic habitats (Korine and Pinshow 2004, Polack et al.
2011), it is invaluable for natural insect control in human habitats. "Bat boxes" have
long been used in successful accommodation of different bat species to human
habitats (Brittingham and Williams 2000, Long et al. 2004).The knowledge of Kuhl’s
pipistrelle’s abundance in urban habitats and its potential benefits as an insect
controller have promoted the use of roosting boxes designed for Kuhl’s pipistrelle
within urban parks in Israel (Herzliya municipality 2009), as has been done similarly
with other insectivorous bats (Rohds 2006, Ibanez et al. 2009). Eradication or
complete prevention of further expansion of Kuhl’s pipistrelle does not only seem
unfeasible (Section 4.1), but also undesirable in certain areas. The strict classical
methodology suggests that the ultimate goal of management, when it comes to
invasive species, is to turn back the clock and restore former species composition
expansion (Wittenberg and Cock 2001, Simberloff 2010). This may be utopian, and in
the real world, it is rarely achieved (Genovesi 2005). A different perspective towards
the management of species' composition was suggested by Rosenzweig (2003, 2005).
Promoting what he calls Reconciliation Ecology, he shows how nature reserves are
too small to maintain biodiversity, due to the log-linear relationship between area and
64
species richness. For this reason, the classical preservation of nature reserves cannot
prevent the possible coming mass extinctions, and the only way to save biodiversity is
by reconciling as many species as we can within human developed areas. Adopting
the concept of reconciliation to my study species, conservation of desert-dwelling bats
will not be guaranteed by classical protection of nature reserves in the Negev, since
current and future development will harm it by facilitating competing invaders.
Allocating conservation resources and research towards the development of open
bodies of water, that will prevent Mediterranean bats from drinking, and thus reduce
the competition with desert-dwelling bats can help sustaining biodiversity. By
focusing on mitigation of the natural bat communities with the outcomes of
anthropogenic development in the Negev, I believe there will be room for all species,
without reducing the valuable enterprise of human settlement in the Negev. This may
well be a better approach rather than tilting at windmills to prevent habitat loss, when
dealing with the challenges that human development presents to conservation. Let us
invest conservation resources in mitigation of the invaded ecosystems, instead of
repeatedly failing to prevent the spread of species into new natural habitats, and then
unsuccessfully trying to eradicate them once they have established.
65
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