Ecosystem Services xxx (xxxx) xxx

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Ecosystem Services
journal homepage: www.elsevier.com/locate/ecoser

Value and benefit distribution of pollination services provided by bats in

the production of cactus fruits in central Mexico
Constance J. Tremlett a, Kelvin S.-H. Peh a, b, Veronica Zamora-Gutierrez a, c,
Marije Schaafsma d, e, *
a
School of Biological Sciences, University of Southampton, University Road, Southampton SO17 1BJ, UK
b
Conservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
c
CONACYT-Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CIIDIR) Unidad Durango, Instituto Politécnico Nacional, Sigma 119
Fraccionamiento 20 de Noviembre II Durango, Durango 34220, Mexico
d
School of Geography and Environmental Science, University of Southampton, University Road, Southampton SO17 1BJ, UK
e
Institute for Environmental Studies (IVM), De Boelelaan 1111, 1081 HV Amsterdam, the Netherlands

A R T I C L E I N F O A B S T R A C T

Keywords: Despite providing important ecosystem services in both natural and agricultural systems in the tropics, bats are
Cash crop often disregarded or considered pests; and research quantifying their importance as pollinators is scarce. We
Columnar cactus quantified the value and benefit distribution of bat pollination in the production of a major fruit crop in Mexico
Economic valuation
(pitayas, Stenocereus queretaroensis). We used exclusion experiments to quantify the effect of bat pollinators on
Ecosystem services
Leptonycteris
crop yield and quality. We then used yield analysis to assess the market value of pollination services, combined
Value chain with value chain analysis to assess the distribution of these economic benefits among actors. Bat pollination
Stenocereus queretaroensis services to pitaya production are worth approximately US$2,500 per ha through increases in both fruit yield and
size, with bats contributing around 40% of gross income across producers. Participation in the pitaya value chain
provides a key seasonal source of cash income at a time of low agricultural activity, supporting livelihoods and
household activities of the rural poor. However, the commercialisation of the pitaya has concentrated economic
benefits with privileged groups who have access to land and markets. Our novel approach to valuing pollination
services is transferable to other crops and pollinator species to demonstrate disaggregated socio-economic
consequences of losing pollinators.

1. Introduction The quantification of ecosystem service benefits in monetary terms is

frequently used to support biodiversity and ecosystem conservation,
Pollinators provide many benefits to humans, improving food pro­ though it is a complex and challenging issue, particularly where services
duction and security, and underpinning biodiversity and crucial are intangible and cannot be valued through existing markets (Adams,
ecosystem functions (Potts et al., 2016a). Nearly 90% of flowering plants 2014; Hanley et al., 2015; Breeze et al., 2016). However, the economic
are reliant on animals for pollination (Ollerton et al., 2011), with three valuation of pollination services, such as the direct contribution of
quarters of leading global crops, particularly those that are richest in pollinators to commercial crop production and quality, can be a useful
micronutrients, showing increases in production or quality when polli­ mechanism to alert decision-makers to the consequences of losing pol­
nated by animals (Eilers et al., 2011; Klein et al., 2007; Potts et al., linators (Hanley et al., 2015). Existing assessments of pollination ser­
2016b). Bats pollinate many plants of high socio-economic value across vices have either focused on the economic importance of insect
the tropics (Kunz et al., 2011). However, bat populations are threatened pollinators, primarily honeybees (Gallai et al., 2009; Winfree et al.,
in many parts of the world, with 80% of bat species requiring research or 2011; Hanley et al., 2015) or have established the role of bats as polli­
conservation attention (Frick et al., 2019), and the value of bats to the nators of tropical crop species, such as durian and fleshy fruits of
maintenance of ecosystems and human wellbeing is largely under­ columnar cacti (e.g. Ibarra-Cerdeña et al., 2005; Bumrungsri et al., 2009;
estimated (Kingston, 2016). Aziz et al., 2017). To our knowledge, none have directly valued the

* Corresponding author at: School of Geography and Environmental Science, University of Southampton, University Road, Southampton SO17 1BJ, UK.
E-mail address: [email protected] (M. Schaafsma).

https://doi.org/10.1016/j.ecoser.2020.101197
Received 21 October 2019; Received in revised form 9 September 2020; Accepted 20 September 2020
2212-0416/© 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

Please cite this article as: Constance J. Tremlett, Ecosystem Services, https://doi.org/10.1016/j.ecoser.2020.101197
C.J. Tremlett et al. Ecosystem Services xxx (xxxx) xxx

effects of bat pollinators on yield and quality of a commercial crop in for a variety of animals (Frick et al., 2014).
economic terms (though see Sheherazade et al., 2019 for a rough esti­ The two main goals of this study are to a) quantify the value of
mation of the value of bat pollination to durian production in pollination services to the pitaya sector in the most important produc­
Indonesia). tion centre, and b) assess how these economic benefits are distributed
One important issue is that, worldwide, ecosystem service benefits – between different actors throughout the pitaya commodity chain.
including those of pollination services – are not distributed equitably Increased awareness of the economic importance of the contribution of
between different social groups (Hassan et al., 2005). Rural and tradi­ bat pollination services may enable local communities and decision
tional populations in poor areas are often more dependent on ecosystem makers to take appropriate actions to ensure the protection of bat
services for their livelihoods and will be disproportionately affected by pollination services. A greater understanding of how these benefits are
declines in pollinator populations (Hassan et al., 2005; Kumar, 2012). distributed intends to inform how future policies can enable more
Subsistence or smallholder farmers are less likely to have the economic equitable access to, and participation in, the pitaya chain.
power to switch to different crops if production fails, or to replace free We use a direct yield analysis approach to estimate changes in both
wild pollinator-mediated services with bought services (Morton, 2007). crop yield and quality between open pollinated and pollinator-excluded
At the same time, the ecosystem service benefits to different stake­ pitaya crops, and use current market prices to value these changes
holders depend on many socio-economic factors, such as market acces­ (Fig. 1). Yield analysis is particularly useful for assessing benefits of
sibility, land rights, and opportunity costs of labour and land pollination services at a local level, directly capturing the benefits of
(Shackleton et al., 2008). While access to ecosystem services can have an pollination services to a crop and differences between cultivars (Breeze
equalising impact on rural households, where there are constraints to et al., 2016; Potts et al., 2016b). However, only benefits accruing
access, some groups may be further marginalised (Kamanga et al., directly to the producer are measured using this method. We therefore
2009). There is a considerable gap in the literature concerning the dis­ use value chain analysis to assess how the economic benefits are
tribution of ecosystem service benefits across different stakeholders, distributed among different actor groups, affecting livelihoods and
particularly in Latin America; and a subsequent need for disaggregated wellbeing more widely (Bolwig et al., 2010; Schaafsma et al., 2014;
analysis to identify constraints and improve access (Carpenter et al., Fig. 1).
2006; Daw et al., 2011; Breeze et al., 2016; Laterra et al., 2019). A value chain describes the system and processes that occur along the
This paper uses the pollination by bats of an important cash crop in chain of the production of a commodity and is often used to identify
Mexico, the pitaya (Stenocereus queretaroensis) as a case study. Bats in the inequalities and constraints in the chain, particularly from the
Leptonycteris genus are the principal pollinators of S. queretaroensis, perspective of weaker actors (Kaplinsky and Morris, 2002; Meaton et al.,
enhancing both yield and quality of the pitaya crop (Tremlett et al., 2015; M4P, 2008). Assessment of profits earned is a useful mechanism to
2020). Leptonycteris yerbabuenae, the lesser long-nosed bat, and L. nivalis, identify barriers in the chain, as greater barriers to particular roles result
the greater long-nosed bat, are species of nectar-feeding migratory bats in higher profits (Kaplinsky and Morris, 2002). However, it is also
distributed from Central America to the southern U.S.A. (Cole and important to evaluate the returns to labour earned by different actors in
Wilson, 2006). They are important pollinators of columnar cacti and the value chain. The poor must often work long hours to meet household
agaves throughout their range, which play keystone ecological roles in needs, indicating ‘time poverty’ even where daily income is sufficient to
arid ecosystems by providing structural resources, nutrients and water provide wellbeing (Bardasi and Wodon, 2010). In this paper, we use

Fig. 1. Synthesis figure of the valuation approach.

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C.J. Tremlett et al. Ecosystem Services xxx (xxxx) xxx

interview data to assess how income is distributed among actors using 3. Methods and data collection
distribution of profits and hourly wages as indicators of inequality. We
then assess the constraints faced to access more profitable roles and We conducted our fieldwork in Techaluta de Montenegro (20.074◦ ,
suggest potential mechanisms to encourage fairer participation in the − 103.550◦ ) during 2016 and 2017. Section 3.1 summarises the exclu­
chain by actor groups. sion experiments we carried out to generate empirical data on changes
in yield and fruit size between openly pollinated and pollinator-
2. Study system excluded pitaya crops. Next, we collected quantitative production and
marketing data from 61 pitaya producers (Section 3.2). We combined
2.1. Study site these data to estimate the economic value of bat pollination to the pitaya
sector in Techaluta de Montenegro (Section 3.3). Then, to assess the
In Mexico, 85% of all cultivated plant species are at least partly distribution of economic benefits resulting from bat pollination services,
dependent on animal pollinators; this, combined with high poverty we analysed economic data collected through structured interviews with
levels and population densities, means that pollination services are a sample of representatives from each actor group involved in pitaya
crucially important to a large component of the population (Ashworth production (Sections 3.2. and 3.4).
et al., 2009). Most columnar cacti (Cactaceae) are highly dependent on
bats for pollination, including all 22 members of the Stenocereus genus, 3.1. Effect of bat pollinators on pitaya crop yield and quality
which have been widely utilised for fruit production in Mexico since pre-
Hispanic times (Casas et al., 1999; Kunz et al., 2011). However, polli­ We carried out exclusion experiments in 2016 to estimate crop yield
nating bat species continue to be threatened in Mexico by land use and under several pollination systems, whereby different flowers were
climate change, mining, and disturbance at roost sites (Zamora-Gutier­ exposed to certain pollinators using bags of different mesh sizes placed
rez et al., 2018; Frick et al., 2019). during the day or at night. This method has been used to determine
Techaluta de Montenegro is one of the most important areas for the effective pollinator taxa in many columnar cacti species in Latin America
commercial production of the pitaya, the fruit of Stenocereus queretar­ (e.g. Molina-Freaner et al., 2004; Ibarra-Cerdeña et al., 2005). Bags
oensis, a species of arborescent columnar cactus endemic to central- made from a very fine mesh excluded all pollinators, and bags made
western Mexico (Ibarra-Cerdeña et al., 2005; Pimienta-Barrios and from 2 cm2 mesh excluded vertebrate pollinators but allowed insects. Six
Nobel, 1994). Home garden cultivation of S. queretaroensis has occurred different treatments allowed us to distinguish between diurnal verte­
since the late 1800s, while intensive commercial production of pitayas brate pollinators, diurnal insect pollinators, nocturnal vertebrate polli­
began in the 1970s (Pimienta-Barrios, 1999). Low input requirements of nators, and nocturnal insect pollinators; with open (all pollinators had
water, fertilisers and pesticides result in a substantial financial return access to the flower) and closed (no pollinators had access to the flower)
(Pimienta-Barrios, 1999). Additionally, the tolerance of S. queretaroensis pollination controls. We studied wild individuals of Stenocereus quere­
to drought and poor soils, as well as the production of fruit in the dry taroensis (n = 30), as well as three different cultivars chosen for their
season when other crops are scarce, make it a sustainable crop in the arid economic importance: Blanco (n = 22), Mamey (n = 30) and Tenamaxtle
production area (Pimienta-Barrios and Nobel, 1994). (n = 27). We placed each treatment on a separate flower on each cactus
The municipality of Techaluta de Montenegro has an area of 79 km2 individual. We monitored flowers under each pollination treatment and
(Mejía Rodríguez, 2012), nearly 40% of which is used for agriculture recorded fruit set, then harvested fruits after a standardised number of
(INEGI, 2009). The main crops by registered volume (tonne) produced in days (52, 57, 54 and 52 days for Blanco, Mamey, Tenamaxtle and wild
Techaluta de Montenegro are alfalfa (13726 t), hay/pasture (4496 t), fruits, respectively) and weighed them. We used estimates from a
maize (3173 t), pitaya (719 t), avocado (700 t), sorghum (484 t) and binomial generalised linear mixed effects model to calculate the prob­
squash (329 t) (SIAP, 2018). The pitaya generates the highest price per able increase in fruit set with bats relative to diurnal pollinators for each
tonne of any crop grown in Techaluta de Montenegro, with a value of cultivar and for wild cacti (for details, see Tremlett et al., 2020).
approximately Mex$19,200 / US$998 per tonne (SIAP, 2018). Regis­
tered pitaya production is expanding yearly, increasing by 71% between 3.2. Data collection: Economic valuation and value chain analysis
2003 and 2018, from 420 t to 719 t (SIAP, 2018). This growth is driven
by an increase in area under production (56 ha registered in 2003 to 86 We identified actor groups involved in the production of pitayas in
ha in 2017; SIAP, 2018). Figures for both pitaya production and value Techaluta de Montenegro using semi-structured interviews with key
are underestimates however, as much production is not officially informants, people previously identified to have expert or broad
registered with the government. knowledge about the pitaya production sector (Newing, 2010). During
the production season in 2017, we collected contact details of potential
2.2. Pitaya value chain participants from each actor group by approaching actors at random in
both the production area (Techaluta de Montenegro) and subsequent
The key stages in pitaya production are cultivation, processing market areas (e.g. Guadalajara). We also used a snowball sampling
(harvesting, peeling fruits, making products), marketing, and con­ technique whereby existing participants were asked to recommend
sumption. Pitaya production in Techaluta de Montenegro is dominated other potential participants. Additionally, we randomly approached
almost entirely by small commercial plantations and home gardens registered producers from a list of 189 provided by the municipality.
(Pimienta-Barrios, 1999). The value chain is short, due to the high We then conducted structured interviews, using a standard set of pre-
perishability of the fruit (fruits must be eaten within one to two days of prepared interview questions (see Supporting Information S3). We asked
harvest) and subsequent localised market (Pimienta-Barrios, 1999). participants for: characteristics of pitaya plantations and harvest; mar­
Most fruits are sold fresh, but a small but increasing proportion is used to keting and fruit prices; a detailed breakdown of financial costs and time
make products. Producers largely sell fruits directly to the consumer, spent on pitaya-related activities by both family members and em­
either at the roadside or at a market. Actors commonly have multiple ployees; and details of socio-economic background. These topics were
functions in the value chain, and the use of intermediaries (defined here selected so we could fully determine aspects of income for each actor
as an agent that buys fruit from producers to sell to vendors) is rare (see group (Kaplinsky and Morris, 2002; Sanogo, 2010; M4P, 2008). To
Supporting Information S1 for a more detailed overview of the stages in validate responses, we asked each respondent several questions relating
the pitaya chain). to total and monthly income, prices and profits. Interviews allowed
accurate data collection while allowing participants privacy to discuss
personal issues (Newing, 2010). We carried out pilot interviews in a

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neighbouring production town (Amacueca) in June 2017 to check and price for all fruits sold by each producer (i.e. the proportion of fruits sold
refine interview questions. per variety was taken as a proxy for the proportion of revenues per
We carried out 124 interviews between July and August 2017. In­ variety), as we did not have data on the number of fruits sold per pro­
terviews were conducted by trained volunteers and lasted between 40 ducer in each price category or per cultivar. In reality, prices received by
minutes and 3 hours. Prior to starting the interview, we provided details producers varied according to both fruit size and time of season; how­
of the project, data storage, and issues relating to anonymity and ever, as producers sold the bulk of their fruits during the peak season for
confidentiality, and obtained written consent from each participant. We one price, and had fruit production dominated largely by one pitaya type
had ethics approval from the University of Southampton ethics com­ (and therefore of a similar size), we deem this assumption defensible.
mittee prior to carrying out data collection. To calculate the value of the fruit quality attributable to bat polli­
nation for each producer, we multiplied proportion of cacti produced of
each pitaya type (YYkww ) by the crop quality dependency specific to each
3.3. Economic valuation pitaya type and producer (Dqkw ). We then summed the change in fruit
quality across pitaya types (K), and multiplied this proportion by the
To estimate the economic value of bat pollination Vb in pitaya pro­
value remaining after subtracting the value of fruit yield attributable to
duction, we used a production value method (Winfree et al., 2011),
bats from gross revenues from pitaya sales, Vw − Vybw . To calculate Vqb ,
which estimates the value of bat pollination assuming that there are no
we then summed the value of the change in quality attributable to bats
substitutes. This economic value is estimated using the following general
across all pitaya producers (W) in the study area, i.e.:
model:
( ( ( )))
( ) Ykw
Vb = D∙P∙Y (1) Vqb = ΣW Vw − Vybw ⋅ ΣK Dqkw ⋅ (4)
Yw
where Vb is the economic value of bat pollination in pitaya fruit pro­ We assigned a null value for unstudied cultivars for both increase in
duction, D is the crop’s dependency on bat pollination (i.e. the fractional fruit yield and size, which accounted for 13% of cacti under production
reduction in crop yield or quality in the absence of bat pollinators), P is overall.
crop price (expressed in Mex$ per fruit) and Y is crop yield (in fruits per To calculate Dqkw , we first collected data on the size of ten fruits in
producer). each of the small, medium and large size bands sold by the roadside in
Our exclusion experiments showed that bat pollination affects both Techaluta de Montenegro in June 2018 to calibrate the weight ranges of
fruit yield (Y), and fruit quality, in terms of size (Q). Thus, there are two fruits in different price categories. We then compared the proportion of
separate elements to the crop’s dependency on pollination: Dyk and Dqkw . fruits in small, medium and large size bands under the nocturnal and
We derived Dyk from the mixed effects model parameter estimates (see diurnal pollination treatments in our exclusion experiments for each
Section 3.1), indicating the difference between pitaya fruit set when bats pitaya type, and calculated the proportion of fruits that would drop to
were excluded (diurnal pollinators only) and fruit set with bats present, lower size bands for each pitaya type k in the absence of bat pollinators
which varies across pitaya types (k). We derived Dqkw from empirical (Table 1). We assumed the most conservative size band changes by
data collected on changes in fruit weights in the absence of bat polli­ minimising the number of size bands dropped by fruits i.e. where a large
nators in exclusion experiments (see Sections 3.1 and 3.3) and the fruit could have become either a medium fruit or a small fruit (as there
subsequent impact on price, which varies across producers (w) and were more fruits in both smaller band without bat pollinators), we chose
pitaya type (k). Hence, Vb has two additive components: a drop of one band rather than two.
The drop in size bands implies that the total value of pitaya fruits V
Vb = Vyb + Vqb (2)
would be lower in the absence of bat pollination because the fruits
would be smaller, and producers would obtain lower prices per fruit. We
where Vyb is the value of the fruit yield attributed to bat pollination (Eq.
weighted prices received by each producer at the beginning, middle and
(3)); and Vqb is the value of the fruit quality attributed to bat pollination
end of the season by the approximate volume sold in each time-band.
(Eq. (4)).
Dependency values were therefore specific to each producer and
To calculate the value of the fruit yield attributed to bat pollination
depended on the weighted prices that each producer could negotiate at
for each producer, we multiplied the proportion of fruits produced of
each size band: for example, a producer that received the same price for
each pitaya type (YYkww ) by the crop yield dependency specific to each
large and medium fruits would have a lower dependency value attrib­
pitaya type (Dyk ). We then summed the change in fruit yield across utable to the decrease in fruit size in the absence of bat pollination than a
pitaya types and multiplied this proportion by the gross revenues from producer that sold large fruits for a higher price than medium fruits. We
selling pitaya fruits (Vw ). To calculate Vyb , we then summed the value of calculated Dqkw by multiplying the percentage of fruits that would
the change in yield attributable to bats across all pitaya producers (W) in change size in the absence of bat pollination for each price-size category
the study area, i.e.: for each pitaya type Sqk by the difference in prices received by each
( ( (
Ykw
)) ) producer. We then summed the differences across the price-size cate­
Vyb = ΣW Vw ⋅ ΣK Dyk ⋅ (3) gories (see Supporting Information S2 for an example of this
Yw
calculation):
Ykw was inferred from total fruit production reported by the producer
multiplied by the proportion of the cultivar/wild cacti under produc­
tion.1 The value of Vybw therefore varies across producers, depending on Table 1
each producer’s total fruit production for each pitaya type (Ykw ), as well Percentage of fruits that moved between each size band in the absence of bat
pollination for each cultivar and wild cacti, based on weights of fruits collected
as their gross revenues from selling the fruits (Vw ). We assumed an equal
from exclusion experiments under nocturnal and diurnal pollination treatments.
Large: Large Large Medium: Medium Small:
1 no → → no → small no
The inference was necessary because producers were unable to provide
change medium small change change
estimates of the total production or revenue per cultivar or the quantity sold per
size (and thus price) category. For each producer, our dataset included: total Blanco 0 9 24 2 9 56
quantity of fruits sold, gross revenues, number of cacti under production per Mamey 33 0 47 0 0 20
Tenamaxtle 6 25 62 0 7 0
cultivar, and average prices per fruit size (small, medium, large) and time in
Wild 0 0 16 0 21 63
season (start, peak, end).

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C.J. Tremlett et al. Ecosystem Services xxx (xxxx) xxx

( )
Pwq0 the two as the per cent increase in profit attributable to increased fruit
Dqkw = ΣQ Sqk ∙ (5)
Pwqb quality with bat pollination. The proportion of income attributable to
bats for product makers was assumed to be equivalent to Dy , as the prices
P
where Pwq0 is the fractional change in price received for each pitaya type of products did not vary according to the size of fruit used to make them.
wqb

for each producer, with Pwq0 indicating the price received per fruit in the We then calculated profit earned by each individual interviewed by
subtracting direct costs incurred by pitaya-related activities (costs of
absence of bat pollination (for size band q0 ), and Pwqb indicating the
renting pitaya plantations, agricultural inputs, salaries and compensa­
price received per fruit with bat pollination (for size band qb ). Sk is based
tions for employees or family members, marketing, transport, tools and
on the information in Table 1, and is the percentage difference in the
equipment, loans, buying pitayas) from gross pitaya income (the sum of
number of fruits moving between each size band q per variety k in the
any income generated by selling pitaya fruits V, pitaya flowers, and/or
absence of bat pollination.
pitaya products, as well as income generated by renting out pitaya
To assess the contribution of bat pollination to employment in the
plantations). Fixed costs e.g. of establishing pitaya plantations were not
pitaya sector, we estimated total extra jobs Jb generated by bat polli­
included in our calculations of costs and profits. For waged workers,
nation by multiplying the total number of employees E of each producer
costs (e.g. commuting, food, tools and equipment, maintenance) were
by the proportion of revenue attributable to bats VVbww . For example, we
subtracted from the hours worked in the season multiplied by the hourly
assumed that a decreased revenue of 35% would result in a workforce wage received.
decrease of 35%. Thus: Finally, we calculated the profit attributable to bats by multiplying
(
Vbw
) profit by the proportion of income estimated to be attributable to bat
Jb = ΣW ⋅Ew (6) pollination services. Estimates of profit attributable to bats involved an
Vw
assumption of constant variable costs per fruit (though we acknowledge
where Jb is total extra jobs generated by bat pollination, and Ew is the that marketing and transport costs will probably not decrease linearly
number of employees of each producer. with decreased production).
To estimate the total gross value of bat pollination services to the To incorporate the number of dependents reliant on pitaya-
pitaya sector in Techaluta de Montenegro, we identified all likely Sten­ generated income across actor groups, we calculated the per capita
ocereus queretaroensis plantations within the municipal boundaries of monthly income of actors by dividing monthly income by the number of
Techaluta de Montenegro, using satellite imagery (Google Earth, 2019). people living in each household. To elucidate the trade-off between
We marked the plantations as polygons and exported them to ArcGIS to profits, working hours and reliance on unpaid labour by family mem­
calculate the area covered in hectares. bers, we calculated the hourly wages of each actor group by dividing
total profit by total hours worked unsalaried on pitaya-related activities
by the respondent or family members,. except for waged workers where
3.4. Value chain analysis fixed hourly wages received are reported.
To understand the importance of pitaya-generated income, we
We used the data collected through interviews with different actors collected data on whether respondents used it for direct household
to understand the production, processing, marketing, and consumption provisioning or were able to save or invest it for long-term benefit, for
stages of the pitaya value chain (Supporting Information S3). To better example by spending it on school fees. We also asked about other income
understand the distribution of economic benefit provided by bat polli­ generating activities throughout the year, and the proportion of yearly
nation services, we assessed the proportion of income attributable to income generated by the pitaya. We evaluated constraints to access
bats, profit, and hourly earnings across actors. profitable roles in the pitaya chain by combining qualitative interview
We first estimated the proportion of income attributable to bats for data with quantitative costs data.
each actor. For all actors that produced fruits themselves we extracted We tested for differences between groups in profit, hourly wage and
values for the percentage of income attributable to bats from changes in per capita monthly income with a Kruskal-Wallis test followed by non-
both yield Dyk and quality Dqkw , from our individual level data collected parametric (Dunn) pairwise tests (using R packages ‘FSA’ and ‘rcom­
through interview questions on production and marketing (section 3.3). panion’; Mangiafico, 2019; Ogle et al., 2019). We also calculated the
A mixed model from the exclusion experiment detailed in section 3.1 Gini coefficient of inequality between groups in profit and hourly wage
provided an average estimate of Dy for individuals that did not produce (using R package ‘DescTools’; Signorell, 2019). Statistical analysis was
fruits themselves. For actors whose income depended on the quantity done in R v. 3.5.3., using R packages ‘dplyr’, ‘tidyr’ and ‘Rmisc’ (Hope,
but not quality of pitaya fruits, we assumed the proportion of their in­ 2019; R Core Team, 2019; Wickham and Henry, 2019; Wickham et al.,
come attributable to bats was equivalent to Dy . This was assumed for 2019).
waged workers (work availability depends on fruit volume, but we had
no data on the specific volumes of fruits of each cultivar handled by their 4. Results
employers) and plantation owners that rented plantations to others (rent
is calculated by number of fruits). For actors whose income depended on 4.1. Economic value of bat pollination service to pitaya production in
both quality and quantity of fruits (e.g. intermediaries and all types of Techaluta de Montenegro
vendors), but that did not produce fruits themselves, we calculated
profit margins for small, medium and large fruits during peak produc­ Pollination by bats resulted in a greater probability of fruit set
tion (as the bulk of fruits are sold during this time) by subtracting costs compared to other taxa in our exclusion experiment, increasing overall
of buying fruits from prices received when selling fruits. We then probable yield by 35% when averaged across cultivars and wild cacti
inferred the overall volume of fruits of each cultivar in the market from (GLMM: χ2 = 286.7, p < 0.0001; Tremlett et al., 2020). However, the
the overall proportion of each cultivar under production across our dependence on bats for fruit set varied between cultivars. Yield
sampled producers; and used data collected in section 3.3 on the pro­ increased by 27% for Mamey (GLMM: p < 0.001) and 35% for wild in­
portion of fruits of each cultivar in each of the small, medium and large dividuals (GLMM: p = 0.002), but there was no effect of bat pollination
size categories (Table 1) to estimate the overall proportions of fruits in on yield for Tenamaxtle (GLMM: p = 0.65) and Blanco (GLMM: p = 0.60)
the market of each size category with and without bat pollination. We individuals. Crop dependency on bat pollination Dyk was therefore 0.27
multiplied the proportion of fruits in each size category by the profit for Mamey, 0.35 for wild, and zero for Blanco and Tenamaxtle in­
margin calculated for each actor, in scenarios of selling 100 fruits in both dividuals; and 0.35 when averaged across cultivars Dy . Neither the
bat pollinator presence and absence, and took the difference between

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C.J. Tremlett et al. Ecosystem Services xxx (xxxx) xxx

closed pollination nor pollination by nocturnal insects treatments producers. Producers with a higher proportion of Mamey and wild cacti
resulted in fruit set. were more dependent on bats for total income, because fruit yield
Fruit weight decreased by 46% in the absence of bat pollination increased with bat pollination relative to diurnal pollination for Mamey
across all exclusion experiment fruits (excluding the two treatments that and wild cacti, but not Tenamaxtle and Blanco. Additionally, producers
did not set fruit and could therefore not be included in analyses of crop that received higher prices for large Mamey and Tenamaxtle fruits than
quality). The dependence of the pitaya crop on bat pollinators for quality medium or small fruits benefited more from bat pollination, as fruits
Dqkw varied with producer, as it depended on the price charged for fruits dropped one or two size-price bands in the absence of bat pollination.
of different sizes, but the impact on price was highest for Mamey and We estimate that income attributable to bats for the 61 producers
Tenamaxtle cultivars, which dropped one or two price bands when bats interviewed generated approximately 129 extra jobs further down the
were excluded (Table 1; Fig. 2a). production chain (e.g. peelers, harvesters), though we acknowledge that
Of the 61 pitaya producers interviewed, 39 owned pitaya planta­ job creation is not linearly associated with income. The number of paid
tions, 40 rented pitaya plantations and 20 owned home gardens (some workers employed by producers ranged from 0 to 33.
respondents produced fruit under more than one system). The total area We classified 190 ha of pitaya plantations within the municipal
under production for each producer ranged in size from 0.03 to 12 ha boundaries of Techaluta de Montenegro from satellite images. This is
(mean = 2.58 ha), and fruit production Yw ha− 1 ranged from 4,200 fruits likely to be an underestimation of the likely total area, as we could not
ha− 1 per season to 633,300 (Table 2). The most commonly managed distinguish spatially dispersed wild cacti and cacti grown in home gar­
cultivars of Stenocereus queretaroensis were Mamey (63% of total cacti dens. Thus, we conservatively estimate the total gross value of bat
under production across producers interviewed), Tenamaxtle (7%) and pollination services to the pitaya in Techaluta de Montenegro to be
Blanco (7%); as well as wild cacti (10%). approximately Mex$9,200,000, ranging between Mex$315,000 and
Bigger fruits command higher prices than smaller fruits (Fig. 2b). Mex$46,800,000 (US$480,000: between US$16,500 and US
Vendors separate fruits into large, medium and small categories, with $2,450,000).
some adding categories at the extreme (tiny, jumbo). There is no mini­
mum size for a pitaya fruit to enter the market. No other fruit charac­ 4.2. Value chain analysis
teristics (e.g. cultivar) affected fruit price at markets we visited. Weights
of small fruits measured at markets in 2018 ranged between 21.7 and 4.2.1. Income and employment
42.1 g (n = 10), medium fruits between 56.3 and 69.5 g (n = 10), and Jobs generated by pitaya production are a chief source of employ­
large fruits between 68.1 and 90.6 g (n = 10). Fruit prices are highest at ment in an area lacking many other opportunities and provide an
the beginning of the season (late May), when there is less fruit available important source of income and a strategy to diversify livelihoods (see
and consumer demand is greatest (Fig. 2b). Prices are lowest during Table S3 for a description of all actors and their roles). The pitaya was
peak production (June). cited as the principal source of income by 49% of respondents, though
Increased fruit yield resulting from bat pollination across the 61 only one household was completely reliant on the pitaya; all other
producers interviewed had a mean total value (before costs) Vybw of Mex households had multiple income streams. Participation in the pitaya
$39,900 per producer (range: Mex$600 to 320,300 / US$32 to 16,700; chain is therefore a ‘gap-filling activity’ for most people: one that pro­
Table 2). The mean value of increased fruit size resulting from bat vides a seasonal income during the period of low agricultural activity,
pollination Vqbw was Mex$39,500 (range: Mex$0 to 298,400 / US$0 to thus increasing its relative importance and compatibility with other
12,500; Table 2) per producer interviewed. Thus, by increasing fruit livelihood activities (Marshall et al., 2006). The actor groups most
yield and size, bat pollination has a mean total market value Vbw of Mex heavily dependent on pitaya-generated income over the year, and
$79,300 per producer, or Mex$48,400 (US$2,530) per ha (range: Mex therefore bat pollination services, were intermediaries and market
$1700 to 246,400 / US$87 to 12,900; Table 2). vendors (an estimated 55% and 46% of yearly income respectively),
The percentage of gross crop value attributable to bat pollination with waged workers reporting between 15% (drivers) and 26% (har­
ranged from 5% to 58% across interviewed producers, with bats vesters) of yearly income coming from work with pitayas (Table 3).
contributing a mean 39% (±12 SD) of gross revenues from fruit sales per However, the pitaya chain is characterised by informal, verbal con­
producer (Table 2), or 42% of total gross income summed across tracts: just 33% of fruit sellers and 45% of waged workers had a contract
arranged prior to the fruiting season, and all were verbal. Participation

Fig. 2. a) Changes in fruit weight observed in exclusion experiments in 2016 between diurnal and nocturnal pollinators. Red dashed lines indicate lower weight
boundaries of different price classes observed in markets in 2018 (small, medium and large); b) final prices (charged to the consumer) of fruits of different price
classes (small, medium and large) at different times of the season in 2017: start = late May; peak = June; end = early July.

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C.J. Tremlett et al. Ecosystem Services xxx (xxxx) xxx

Table 2
Characteristics of pitaya production and value of bat pollination services across the 61 interviewed producers.
Size of plantation, ha Yw ha− 1, # fruits Vw, Mex$ Price of a small fruit1, Mex$ Price of a medium fruit1, Mex$ Price of a large fruit1, Mex$

Mean ± SD 2.58 ± 2.83 51,547 ± 90,914 187,895 ± 254,146 2.0 ± 1.0 3.5 ± 1.2 5.0 ± 2.0
Range 0.03–12.00 4233–633,333 4,500–1,350,000 0.5–5.2 2.0–7.3 1.9–10.5

Ybw, # fruits Vybw, Mex$ Vqbw, Mex$ Vbw, Mex$ Vbw ha− 1, Mex$ % V attributable to bats

Mean ± SD 12,447 ± 18,743 39,861 ± 59,915 39,460 ± 58,356 79,321 ± 116,023 48,405 ± 53,112 39 ± 12
Range 335–94,920 610–320,355 0–298,399 610–618,754 1660–246,393 5–58
1
Prices weighted by approximate volume sold at different times during the season (different prices are received by farmers at the beginning, middle and end of the
season; see Fig. 2b). Yw ha− 1: total number of fruits produced each year (yield) per hectare. Vw: gross revenues from fruit sales. Ybw: total yield attributable to increase
in fruit set with bat pollination relative to other taxa. Vybw: total value of yield increase with bat pollination per producer. Vqbw: total value of size increase with bat
pollination per producer. Vbw: total value of yield and size increase with bat pollination. Vbw ha− 1: value of bat pollination per hectare of pitaya plantation. %V:
percentage of gross revenues from fruit sales attributable to increases in yield and size of pitayas due to bat pollination.

in the pitaya value chain thus precludes permanent, formal work with (54%), investment back into pitaya or other businesses (40%), savings
benefits such as health insurance and pensions that only accrue to (37%), household goods (36%), children’s education (30%) and other
workers in continuous employment, creating a lack of social security for uses including medical bills and paying debts (19%). Little pitaya-
most actors. Despite this, the lack of technical entry requirements, generated income is passed onto the government (7%) as few taxes
instant generation of cash at low times of the year, and higher wages are paid; most government revenue results from actors buying petrol
relative to other low-skilled jobs, makes the pitaya sector an attractive from the state-owned distributor (Table S5). External agents, for
employment option for resource-poor people. Working with pitayas of­ example suppliers of packaging or agricultural inputs, accounted for the
fers a higher daily rate during the pitaya season than many other con­ remaining 9% of pitaya-generated income (Table S5).
current available job opportunities, such as agricultural day labouring
(Mex$200 per day) or jobs tending plants in large greenhouses that grow 4.2.3. Profits
berries for the export market (Mex$120 per day). The distribution of profits between actors was unequal (Gini coeffi­
The discrepancy between the highest and lowest mean hourly wages cient = 0.60). The highest profits (income minus direct costs) were
of actors in the value chain (Gini coefficient = 0.67) indicates inequality gained by market vendors who both produced fruits and sold them
in the distribution of both economic benefits and labour costs between directly to the consumer, achieving the highest final fruit prices
actors. The low agricultural requirements of the cacti result in a low (Table 3; Fig. S1). However, intermediaries, producers and plantation
labour cost for landowners, particularly those that rent plantations to owners all earned a higher hourly wage (Table 3) indicating the high
others for the production season. Actors that had multiple functions in labour cost (long working hours) of market vendors. Additionally, many
the value chain, such as market vendors that both produced and sold market areas have become saturated, with vendors citing too much
fruit themselves, commonly worked very long hours of up to 22 hours a competition from other sellers as a primary obstacle to making profit.
day. The mean hourly wage of plantation owners who rented plantations The barriers to accessing the most profitable marketing situations are
to others was 22.6 times higher than that of peelers and 5.4 times higher access to a vehicle and obtaining selling permits. Plantation owners that
than that of market vendors (Mex$543, Mex$24 and Mex$101 per hour rented plantations to others achieved both the highest hourly wage and
respectively; Table 3). the second highest profit. As the plantations require little maintenance
or input of resources, profit margins are good both for owners renting
4.2.2. Costs pitaya plantations out for the season for a fixed sum of money, and for
Wages and benefits are a major cost for all the different actors except those that harvest and sell the fruit themselves.
intermediaries (Table S4). Transport costs (predominantly petrol) and Producers that sold peeled fruits to other vendors could earn very
rent are important costs for marketing actors. The costs incurred by high profits but there was substantial variation across respondents
intermediaries and market vendors are the highest, while plantation (Table 3). Profits earned by this group in our study are biased by one
owners have among the lowest costs, thanks to the low agricultural in­ producer that had a very high production and took the fruits to Gua­
puts required (Table S4). A mean of Mex$1,260 per ha per year (US$66) dalajara to sell direct to market vendors; producers that sold to vendors
was spent on compost, fertilisers, herbicides and pesticides combined. or intermediaries in Techaluta earned much lower profits. The localised
However, there is a high initial fixed cost of establishing pitaya plan­ nature of the pitaya market results in a good level of market information
tations, representing a significant barrier to entry for other actors. throughout the chain and enables direct market access by most actors.
Establishment costs are between approximately Mex$9,460–72,300 per This increases the power of producers to earn a fair price and results in
ha (US$494–3,780 per ha), excluding the price of buying land, con­ intermediaries being uncommon, who frequently earn excessive profits
sisting of the costs of labour and buying cactus branches to plant. in value chain assessments (Marshall et al., 2006). Nonetheless, the few
Furthermore, there is then a lag time before fruit production of up to 10 intermediaries active in the pitaya chain earn a high profit due to the
years. Access to formal credit is low: six percent of waged workers had large number of fruits traded, despite earning the lowest profit margin
access to credit and thirteen percent of non-waged workers. There was on fruits (Table 4) and having the highest costs (Table S4).
no significant difference between actor groups in per capita monthly A substantial part of pitaya-generated profit for all actor groups
income (Table 3), though those that earned the highest (plantation could be attributable to the impacts of bat pollination on crop yield and
owners that rent their plantations out to other people, Mex$3,770 ± quality (Fig. 3a and b). Actors whose profits depended on the quality of
1444 SE) had a per capita monthly income of nearly four times those fruits as well as quantity were more dependent on bat pollination ser­
who earned the lowest (peelers, Mex$1,000 ± 198 SE), indicating that vices than actors who depended on quantity only, as profit margins per
access to land may be captured disproportionately by an already fruit decreased with fruit size (Table 4), and fruits were smaller in the
economically privileged group. absence of bat pollination. Intermediaries, and ambulant, roadside and
The majority of the income (84%) associated with pitayas accrues to market vendors had the largest mean percentage of profits attributable
the local community and is retained as cash income, supporting to bat pollination (62, 56, 47 and 46% of profits respectively; Fig. 3b).
household activities (Table S5). Cash income generated from the pitaya Actors with the highest value of profit attributable to bat pollination
was allocated to: household food (71% of respondents), rent and bills services however, were those that earned the most from working with

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 C.J. Tremlett et al.
Table 3
Income indicators for different actor groups.
1
Actor Peelers* Agricultur-al Ambulant Drivers* Product Harvesters* Home Roadside Plantation owners Market Producers – sell Producers Intermediaries Plantation Kruskal –
workers* sellers makers garden vendors -do not rent out vendors fruit with spines – sell owners – rent Wallis test 3
owners peeled fruit out

N 12 6 5 4 9 11 20 31 30 19 8 4 4 9
Income indicators based on calculations in section 3.4:
ab a
Wage/ 17,201 7,500 45,156 bcd 10,369 ab
27,277 abc
12,126 a
49,751 bc
57,531 c
78,083 cd
125,590 d
17,505 ab
127,099 96,419 cd
102,409 cd χ2 = 64.2,
bcd
Profit*, ± 3,856 ± 2,869 ± 6,214 ± 5,331 ± 7,048 ± 1,413 ± 11,717 ± 13,818 ± 18,504 ± 24,979 ± 7,350 ± 47,984 ± 51,970 df = 13,
Mex$ ± SE ± 90,386 p < 0.0001
Hourly 24 b 25 ab 31 ab 32 abc 35 ab 39 abc 47 ab 47 b 90 ab 101 abc 125 abc 165 abc 183 ac 543 c χ2 = 34.2,
wage ±2 ±0 ±8 ±9 ±8 ±7 ±8 ± 12 ± 25 ± 24 ± 55 ± 135 ± 61 ± 234 df = 13,
Mex$ ± SE p ¼ 0.001
Income indicators based on answers to interview questions:
Per capita 1003 1327 1410 1234 2003 1436 1664 1459 2150 2921 1881 1879 2917 3767 χ2 = 11.0,
monthly ± 198 ± 217 ± 370 ± 115 ± 653 ± 228 ± 382 ± 220 ± 409 ± 871 ± 189 ± 221 ± 896 ± 1444 df = 13,
income p = 0.61
8

Mex$ ± SE
2
Per cent 23 23 23 15 33 26 35 36 45 46 32 35 55 37
yearly
income
from
pitaya
1
The majority of respondents belonged to multiple actor groups, so individual data may be used for several groups (e.g. plantation owners that are also market vendors). Product makers here are those that did not also
sell fruits (i.e. were solely product makers). Producers here are those that produce fruit but do not sell it directly to the consumer, but instead to another vendor or intermediary, either peeled or with spines. *Waged
workers.
2
Per cent of yearly income from the pitaya calculated from the average category rank that actors reported during interviews in answer to the question “What percentage of your average annual income comes from the
pitaya?” (1 = 0–20%, 2 = 20–40%, 3 = 40–60%, 4 = 60–80% and 5 = 80–100%). The mid-point of each category range was used.
3
Different letter superscripts indicate significant differences between mean incomes based on non-parametric (Dunn) pairwise tests at p < 0.05, using the Benjamini and Hochberg correction (using R packages ‘FSA’ and
‘rcompanion’ Mangiafico, 2019; Ogle et al., 2019).

Ecosystem Services xxx (xxxx) xxx

C.J. Tremlett et al. Ecosystem Services xxx (xxxx) xxx

Table 4 and relevant information to decision makers (Ninan and Inoue, 2013).
Profit margin (Mex$) per fruit of each size category during peak production The value of pitaya-generated income is significant in an area where
(±SD) for actors buying fruit to sell rather than producing their own (cost of 49% of people have an income insufficient to provide wellbeing (CON­
buying fruit subtracted from sale price received for fruit). EVAL, 2010). Among individual pitaya farmers within our study region,
Small (Mex$) Medium (Mex$) Large (Mex$) we found considerable variation in dependence on bat pollination for
Intermediaries 0.3 ± 0.3 0.6 ± 0.4 1.1 ± 0.8 income, highly impacted by the cultivars grown and the prices charged
Ambulant vendors 1.5 ± 0.4 2.3 ± 1.1 3.6 ± 1.2 for fruits of different sizes. However at the community scale, our
Roadside vendors 1.3 ± 2.5 3.3 ± 1.8 4.3 ± 1.1 research showed pitaya production to be heavily dependent on bats,
Market vendors 2.5 ± 0.0 4.1 ± 0.5 6.8 ± 2.5 particularly that of the most economically important cultivar, with the
spatial and genetic structure of pitaya plantations likely exacerbating
pitayas: market vendors, producers and plantation owners (Fig. 3a; the reliance on bat pollinators (Tremlett et al., 2020).
Table 3). Our multi-faceted approach to estimate the value and distribution of
pollination services may be useful for other animal-pollinated crops,
5. Discussion particularly those in less formal markets where a lack of registered data
on crop production or the value chain necessitates the collection of
Our study used an interdisciplinary approach to examine both the primary data. We found that pollinator-mediated changes in fruit quality
value of the direct impacts of bat pollination on crop yield and quality, had a high impact on the estimated value of pollination services,
as well as a disaggregated analysis of the distribution of the economic demonstrating the importance of conducting detailed field experiments
benefits among actors. We found the value of bat pollination services to to generate empirical data on the dependency of both crop quality and
be worth approximately US$480,000 in the municipality of Techaluta de yield on different pollinators, as well as including multiple cultivars in
Montenegro alone, highlighting the great importance of bat pollinators study designs (Melathopoulos et al., 2015).
for the welfare of the rural production region, and the severe economic Additionally, we have shown that value chain analysis is a useful
consequences should bat pollinator populations decline. approach for the evaluation of the social distribution of economic ben­
Leptonycteris yerbabuenae populations suffered severe declines in the efits received from ecosystem services, allowing explicit analysis of in­
1980s, resulting from persecution and disturbance at roosts and loss of equities in income among actor groups and constraints to access roles
foraging habitats (Medellín, 2016). A conservation recovery programme (Gundimeda et al., 2018; Zhang et al., 2018). To our knowledge there
has successfully used environmental education and roost protection has been no such attempt to disaggregate benefits from pollination
schemes to increase population sizes, resulting in delisting of the species services between actors for any crop (Suich et al., 2015). We found that
by both the Mexican and US governments (Trejo-Salazar et al., 2016; US access to the bat pollination service did not have an equalising impact,
Fish and Wildlife Service, 2018); though the species remains classified with some actors receiving a disproportionate share of economic benefit
Near Threatened by the IUCN Red List (Medellín, 2016). However, it is or labour costs, and the chain characterised by a lack of social security
vital that public awareness of the ecosystem services provided by bats throughout. The change of the pitaya from a communally collected
continues, such as the contribution of bats to food security. This is resource to an individually owned commodity may disadvantage poorer
particularly pertinent in the light of the recent Covid-19 pandemic that actors who lack the land or capital to establish plantations themselves or
has widely negatively associated bats with the virus, driving new threats access profitable markets, despite an overall increase in economic
to bat populations (Fenton et al., 2020; Zhao, 2020). Our own recent wellbeing at the community level (Marshall et al., 2006; Kamanga et al.,
engagement with inhabitants of the pitaya production area indicates 2009). Laterra et al. (2019) found a lack of financial capital to be the
growing concern about subsequent negative public perceptions of bat- most important source of inequality in access to ecosystem services
pollinated fruits. across Latin America; inequality then increases over time as access to
Economic valuations are one way of raising awareness of the unseen land gradually decreases with resource commercialisation. At the same
benefits of bats, with local context-specific research providing useful time, the ease of entry to the pitaya chain (low technical entry re­
quirements, a local market) may lead to excessive competition between

Fig. 3. a) The profit in Mex$ attributable to bats (±SE) across actor groups, calculated by multiplying profit by the proportion of income attributable to bats for each
actor (for waged workers, ‘profit’ is wage received multiplied by hours worked, minus costs), and b) the mean percentage of pitaya-generated income estimated to be
attributable to bats for each actor group.

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C.J. Tremlett et al. Ecosystem Services xxx (xxxx) xxx

small-scale producers and vendors in the production area, limiting the pollination of a highly valuable agricultural product.
profitability. Additionally, the production value method assumes that crop prices
will be unaffected by decreased supply in the case of pollinator loss, and
5.1. Conservation and policy implications that farmers cannot compensate for reduced pollination supply by
reducing input costs or employing substitutive pollination (Winfree
Communicating the economic benefits provided by bats helps to et al., 2011). Techaluta de Montenegro contributes 40% of registered
raise awareness among the public and policy makers of the importance pitaya production in Jalisco (SIAP, 2018) and therefore price increases
of bat conservation actions (Cleveland et al., 2006; Boyles et al., 2011; may be seen with decreased fruit supply. However, the pitaya is already
Kunz et al., 2011). Community environmental education programmes a highly priced luxury fruit, and 67% of consumers interviewed in our
can be an important tool to improve understanding of bats by generating study said that they would buy fewer pitayas if the price increased. Input
more positive attitudes shaped by the benefits bats provide, rather than costs are already low for pitaya producers and it is unlikely they could be
the damage they may cause (for example by vampire bats, Desmodus reduced further without loss of employment. Furthermore, bats are wild
rotundus, which can transmit bovine paralytic rabies to livestock in Latin pollinators that cannot be replaced by a managed service, e.g. from
America) (López-del-Toro et al., 2009; Williams-Guillén et al., 2016). rented bee hives; and the cost of hand-pollination is likely to be pro­
Those actors who benefit the most from bat pollination services may hibitive (Partap and Ya, 2012), though cost estimates are not available
be best placed to contribute to bat conservation practically (e.g. land for this crop.
owners) and economically (e.g. consumers). At a local practical level, It was beyond the scope of this study to consider the distribution of
protection of bat roosts and avoidance of persecution (many bats are benefits received by actors other than income. Poverty and wellbeing are
killed under the mistaken assumption that they are vampires) will complex and context dependent, now commonly described with multi-
benefit bat populations, maintaining both the provision of pollination dimensional factors encompassing human and social deprivations as
services and other bat-mediated ecosystem services such as seed well as economic (Suich et al., 2015). For a better understanding of the
dispersal and pest suppression (Kunz et al., 2011; Williams-Guillén et al., impact of bat pollination services on wellbeing, the effect of pitaya-
2008). Additionally, to maintain the provision of bat ecosystem services generated income on other objective elements of well-being (such as
in pitaya plantations, it is vital that the intensification of the pitaya access to health services), and subjective elements (such as cultural
sector does not result in increased use of pesticides and other agro­ importance or contribution to sense of identity) would need to be
chemicals. Pitaya production currently is largely small-scale and quantified.
organic; however, production is expanding yearly, with attempts to
export the fruits internationally. Pesticide exposure can have various 6. Conclusion
lethal and sub-lethal effects on bats, including disruption of hormones
and the immune system, reproductive failure, and changes to behaviour The consequences of losing bat pollination services to pitaya pro­
(Bayat et al., 2014). We found consumers of pitayas to have a higher duction in Techaluta de Montenegro would be severe. By enhancing fruit
monthly income and level of education than any of the actors involved in production and fruit size, bat pollinators contributed around 40% of the
the production chain (Table S3), suggesting that they can afford to total gross income of interviewed pitaya producers in the area, equiva­
contribute to initiatives such as a ‘bat-friendly’ pitaya label (e.g. see lent to US$2,500 per ha annually. This value reflects the high level of
Trejo-Salazar et al., 2016: bat-friendly tequila). Such initiatives could dependence of the pitaya crop on bat pollinators for both yield and
add a small surcharge to pitaya prices to feed into conservation efforts quality; as well as the high prices achieved for pitayas. The reliance of
such as environmental education programmes or the installation of local employment and income on pitaya production, and thus bat
protection at roost sites. pollination services, is a strong argument for the conservation of bat
Until now, there have been no direct economic valuations of bat populations in the production area. However, our value chain analysis
pollination services provided to crops, though several studies have showed that barriers to access the most profitable roles should be
estimated the value of crop pest suppression by bats. Bat-mediated pest reduced to enable a fairer distribution of economic benefits among ac­
control has been valued between $0 (for coffee and cacao) and $183 tors, which are currently disproportionately captured by groups already
(cotton) per ha, representing 0% and 12% of the total crop value economically or socially advantaged. Our interdisciplinary approach
respectively (Cleveland et al., 2006; Maas et al., 2013; Maine and Boy­ combining exclusion experiments, plantation yield data and value chain
les, 2015; Puig-Montserrat et al., 2015; Taylor et al., 2018). The higher analysis provides a novel basis for valuing the benefits of services by
value of bat pollination (US$2,500 per ha) revealed by our study sug­ other animal pollinators and other crops, as well as the distribution of
gests that this may be a more effective economic argument for bat those services across actors.
conservation in some areas.
This research also has important policy implications for equitable
development. In order to ensure that benefits from bat pollination are Declaration of Competing Interest
distributed more fairly across actors, activities could be started at the
community, government or NGO level, such as: selling fruits or products The authors declare that they have no known competing financial
collectively; opening up new markets (with assistance to cope with any interests or personal relationships that could have appeared to influence
resulting extra certification or tax requirements) or improving access to the work reported in this paper.
existing markets; supporting new actors financially to establish planta­
tions; supporting the introduction of a low-entry health insurance; and Acknowledgements
providing training and equipment to increase product-making capacity.
This work was supported by the Natural Environmental Research
5.2. Limitations, uncertainties and knowledge gaps Council (grant number NE/L002531/1), with additional funding from
the British Cactus and Succulent Society (to CJT), Bat Conservation In­
Fruit set and fruit quality between pollination treatments may vary ternational (to VZG) and the University of Southampton (to CJT and
between years, impacted by fluctuations in climate and pollinator KSHP). We are indebted to all the volunteers for their assistance in the
availability (Melathopoulos et al., 2015). Economic value will also field, to SEDER Jalisco, and all the authorities and inhabitants of the
fluctuate with changes in market prices, and institutional or external municipality of Techaluta de Montenegro who contributed directly or
environmental factors (López-Hoffman et al., 2014). Nonetheless, our indirectly to our work, without whom this research could not have
research has clearly demonstrated the economic importance of bats for happened.

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Appendix A. Supplementary data Kamanga, P., Vedeld, P., Sjaastad, E., 2009. Forest incomes and rural livelihoods in
Chiradzulu District. Malawi. Ecol. Econom. 68, 613–624. https://doi.org/10.1016/j.
ecolecon.2008.08.018.
Supplementary data to this article can be found online at https://doi. Kaplinsky, R., Morris, M., 2002. A Handbook for Value Chain Research, Vol. 113.
org/10.1016/j.ecoser.2020.101197. University of Sussex, Institute of Development Studies.
Kingston, T., 2016. Cute, Creepy, or Crispy - how values, attitudes, and norms shape
human behavior toward bats. In: Bats in the Anthropocene: Conservation of Bats in a
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