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Ejemplo 1
Ejemplo 1
doi: 10.1093/aesa/saaa044
Review Review
Abstract
Malaise traps are important tools for the large-scale collection of arthropod taxa. Here, an extensive review
of the history and literature concerning Malaise and canopy traps is given. This review highlights how trap
design and placement can affect trap catch, which will help researchers to make more informed choices when
planning research endeavors. Additionally, terrestrial and canopy-style Malaise traps are compared to each
other and other types of arthropod traps.
“Since the time of Linnaeus the techniques of catching insects ‘rarefaction curve’, and combinations of those terms. Once rele-
has not improved very much.” vant literature was acquired, additional references were found by
– René Malaise 1937. scouring the citations. Steyskal (1981) and Achterberg (2009) pro-
vided extensive bibliographies on Malaise trap research and were
Malaise traps—which are large, tent-like structures made of fine
invaluable resources. The number of days between specific dates was
mesh netting—are one of the most widely used nonattractant, static
calculated using ConvertUnits (2020).
insect traps (Muirhead-Thomson 1991). They were first devel-
Herein, we use ‘Malaise trap’ to refer specifically to terrestrial
oped by René Malaise after he observed insects trapped inside of
Towne’s style Malaise traps (e.g., those traps set near, or in contact
a tent and provided the first passive method to survey and collect
with, the ground or over streams) and ‘canopy trap’ to refer to those
large numbers of flying insects. Malaise traps take advantage of the
traps suspended at considerable height above the ground, generally
fact that many insect species climb up after encountering a barrier.
in the forest canopy. While Malaise and canopy traps are based on
The traps primarily sample flying insects, especially Diptera and
similar designs and Malaise traps set in different environments (e.g.,
Hymenoptera, which are intercepted by the mesh walls, but also col-
field, forest, and over streams) may sample diversity as different as
lect numerous ground-dwelling species as well (Zilihona et al. 1998,
that sampled by Malaise and canopy traps, we make the distinction
Achterberg 2009).
between Malaise and canopy traps herein as such a distinction is
While Malaise traps are used extensively to survey insects and
made in the published literature. Other styles of Malaise traps (e.g.,
various short reviews have been written about them, there is no
Gressit Malaise traps) are referred to by their full names.
comprehensive review that cites much of the underlying literature.
Herein, we provide a review of Malaise traps, including the history
of their development, commonly collected taxa, factors that influ- History
ence the arthropods collected by the traps, and various uses and René Malaise (1892–1978) was inspired to invent a new type of in-
questions that have been investigated using Malaise traps. We also sect trap after watching insects fly into a tent and become trapped
compare Malaise traps to other arthropod survey methods and com- despite the open flaps. His design consisted of mesh fabric stretched
ment on potential problems concerning the use of Malaise traps. We over a wooden box frame open at one end with a collection cylinder
hope that this review will serve as a resource for anyone who uses at the top (Fig. 1; Malaise 1937). It would revolutionize the collec-
Malaise traps to collect insects. tion of flying insects.
Vecht (1939) was the first person to utilize Malaise’s design when
he successfully tested it in Burma and translated the design into
Material and Methods Dutch. However, it is unclear if his contribution had much impact
The first author conducted an extensive literature search on Google on the history of the trap design.
Scholar for terms such as ‘Malaise trap’, ‘canopy trap’, ‘SLAM trap’, Henry Townes (1913–1990) elaborated upon Malaise’s design
arthropod order and family names (e.g., ‘Diptera’ and ‘Tachinidae’), and presented a modified version of the trap at the 1959 Annual
© The Author(s) 2020. Published by Oxford University Press on behalf of Entomological Society of America. 1
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2 Annals of the Entomological Society of America, 2020, Vol. XX, No. XX
traps in the canopy much easier and is now the design used almost
exclusively in such studies. collector depending on whether the trap is set in the understory or
Malaise traps have been combined with other traps, including canopy (Vance et al. 2007). However, the bottom collector may
light traps (Dufour 1980), window traps (Basset 1988; Fig. 6), and interfere with the collection of certain taxa (e.g., Cerambycidae), so
intercept traps, including colored pan traps (Fig. 7), in order to it may not be appropriate to always include one (DiGirollomo and
modify taxa collected or increase efficiency. The addition of yellow Dodds 2017).
pan traps beneath Malaise traps increases the trap effectiveness in Wet or dry killing agents may be used in the collecting head.
catching Diptera, Hymenoptera, Heteroptera, and Thysanoptera Both have advantages depending on the taxa targeted. Wet killing
(Darling and Packer 1988, Campos et al. 2000). Henry et al. (2018) agents—such as 70–90% ethanol or propylene glycol—also function
presented an ‘alpine Malaise trap’, which consists of two interlocking as a preservative, which is needed if traps are serviced on a weekly
clear plastic panes rather like a flight intercept trap, that can be com- or longer basis. Delicate specimens, especially Lepidoptera, may be
bined with a drop trap or colored sticky cards for use in windy, high- damaged by wet killing agents and unidentifiable beyond higher
altitude environments. taxonomic levels (e.g., family or genus). Dry killing agents—such
as naphthalene and insecticide-permeated strips—help alleviate this
Trap Setup and Implementation but require traps be serviced more often, potentially daily, as insects
Malaise traps can be erected in any location where flying insects are may damage themselves or other specimens before succumbing to
expected, including forests, open grassy areas and prairies, and wind- the killing agent, especially if an excess of specimens builds up in the
swept ridges, although care must be taken to secure them when high trap head. If interested in ectoparasites or phoretics present on flying
winds are expected. Trap location affects the taxa collected (Ozanne insects, dry killing agents have shown to be effective at killing the
2005). Insects often follow specific flight paths through vegetation ectoparasites on-host, often preserving the host–symbiont relation-
and a trap located along a flight path will catch more specimens than ship. Wet killing agents often result in detachment of the symbiont
one that is not (Matthews and Matthews 1983, Hutcheson 1990, and mixing of symbionts among individuals in the collection jar.
Southwood and Henderson 2000). Traps set in sunny, exposed areas
collect more insects than those in sheltered, shaded areas (Noyes 1989, Taxa Collected
Irvine and Woods 2007). Topography, wind, water, light, and other Diptera and Hymenoptera are generally the numerically dominant
abiotic conditions should also be taken into consideration (Gressitt taxa in Malaise traps, with Diptera often representing the majority
and Gressitt 1962, Richards and Windsor 2007). Additionally, some of specimens collected (Table 1). Because of this, Malaise traps are
researchers have suggested setting traps in a north-south orientation often used to generally survey diversity of diptera diversity. However,
with the trap head facing the sun’s zenith (Noyes 1989). they have also been used to specifically collect and survey many spe-
While environmental factors have been little studied, Matthews cific Dipteran taxa, including Tabanidae, Syrphidae, and Tachinidae
and Matthews (1969) reported temperature and precipitation had a (Table 2). Hymenoptera are generally the second most-collected
strong influence on trap catch, with the largest catches happening on taxa, though usually represent a much smaller percentage of the
hot, sunny days following rain. total catch than flies. Similar to Diptera, Malaise traps are often
The addition of a bottom collector to canopy traps can be im- used to survey general hymenopteran diversity but have also been
portant, as some taxa are preferentially caught in the top or bottom used to target specific taxa, including Braconidae, Ichneumonidae,
4 Annals of the Entomological Society of America, 2020, Vol. XX, No. XX
and Vespidae (Table 3). Besides Diptera and Hymenoptera, Malaise sequences of one of a few genes to identify the taxa in a sample
traps have been used to collect a variety of Arachnida, Odonata, (Aagaard et al. 2016, Geiger et al. 2016, Morinière et al. 2016,
Coleoptera, Lepidoptera, and other insects (Table 4). Canopy traps Aagaard et al. 2017, Cancian de Araujo et al. 2017, Schmidt et al.
have been used to specifically collect Psocoptera, Thysanoptera, 2017, Cancian de Araujo et al. 2018, Watts et al. 2019).
Coleoptera, Diptera, Lepidoptera, Neuroptera, and Hymenoptera Malaise traps have been shown to be some of the most consistent
(Table 5). traps in terms of the composition of higher taxa collected, giving
Malaise traps run with wet collecting heads are generally con- credence to the confidence hymenopterists and diperists have that
sidered to be a poor choice when targeting Lepidoptera, as many they will invariably collect those taxa (Kitching et al. 2001). While
specimens lose their scales in liquid preservative (Walker and Crosby such consistency has not been studied in canopy traps, there is no
1988, Brown 2005, Krogmann and Holstein 2010). However, a reason to believe they do not sample similar groups irrespective of
number of studies have used Malaise trap-caught Lepidoptera for site locality.
genitalia studies (Schmidt 2014a,b, 2016, 2017; van Nieukerken
et al. 2016) and Schmidt et al. (2019) proposed a workflow for cur-
ating wet Lepidoptera that can be used to prepare pinned moths Application in Entomology Field Studies
and butterflies. Additionally, DNA work can still be conducted on Malaise traps are excellent tools for surveying biodiversity (e.g.,
wet lepidopterans, including metabarcoding of Malaise trap sam- Collections Unit 2017, Karlsson et al. 2020), especially when used
ples, which uses high-throughput DNA sequencing targeting short in conjunction with traps that collect nonoverlapping assemblages
Annals of the Entomological Society of America, 2020, Vol. XX, No. XX 5
2008, Rohr et al. 2009, Banks et al. 2010, Sellars and Hicks 2015,
Carey et al. 2017, Wolton et al. 2017, Pérez-Urbina et al. 2018,
Westwood et al. 2018). Additionally, Malaise and canopy traps have
been used to investigate community differences in monospecific and
highly diverse tree canopies in agroforestry (Sperber et al. 2004),
how arthropod communities change during plant succession (Hollier
and Belshaw 1992, Hutcheson 1999, Shlyakhtenok and Agunovish
2001, Nol et al. 2006, Missa et al. 2009, Rohr et al. 2009), crop
stage (Silva et al. 2020), stand growth (Hutcheson and Jones 1999,
Luqman et al. 2018), invasion by foreign plant species (Toft et al.
Malaise and canopy traps can be used to estimate the abundance Buskirk 1975, Kato et al. 2003, Kato et al. 2004; Odonata: Kirkton
of target pest species (Beggs et al. 1998), establish damage thresh- and Schultz 2001; Anura: Horn et al. 2005; Chiroptera: Jong and
olds (Beggs and Rees 1999), or create an index of abundance, avail- Ahlen 1991, Fukui et al. 2006; Aves: Poulin et al. 1992, Rodenhouse
ability, and biomass of captured arthropods by themselves or as a and Holmes 1992, Duguay et al. 1997, Duguay et al. 2000, Johnson
prey base for insectivorous predators (Lynch et al. 2002; Araneae: and Sherry 2001, Kwok and Corlett 2002, Murakami and Nakano
Annals of the Entomological Society of America, 2020, Vol. XX, No. XX 7
Table 2. Diptera families collected in Malaise traps Table 3. Hymenoptera taxa collected in Malaise traps
General Diptera Kitching et al. 2004, Roháček and Ševčik 2009, General Hymenoptera Darling and Packer 1988, Noyes 1989, Campos
Wolton et al. 2017 et al. 2000, Shlyakhtenok 2000, Sobek et al.
Agromyzidae Scheirs et al. 1997; Papp 2009, 2018 2009
Axiniidae Colless 1994 ‘Symphyta’ Holuša 2002, Brand et al. 2003, Harris 2006
Asilidae McCracy and Baxa 2011, McCravy 2017, Aculeata Volpato et al. 2019
Martín-Park et al. 2018 Apocrita Karem et al. 2006
Brachystomatidae Plant et al. 2020 Apoidea/Anthophila Bartholomew and Prowell 2005, Ngo et al.
Table 4. Arthropod taxa, excluding Diptera and Hymenoptera, col- Table 5. Insect taxa collected in canopy traps
lected in Malaise traps.
Taxon Reference
Taxon Reference
Psocoptera Santos et al. 2007, Sokolova
Acari Zheng 1996; Behan-Pelletier and Winchester et al. 2010
1998; Clark 2004; Zheng 2002a, b; Ripka Thysanoptera Santos et al. 2007
and Szabó 2010; Skvarla et al. 2014 Coleoptera Tangmitcharoen et al. 2006,
Araeneae Wilkinson et al. 1980, Hauge and Midtgaard Hardersen et al. 2014
1986, Jennings and Hilburn 1988, Cerambycidae Vance et al. 2003, Dodds et al. 2010,
Oxbrough et al. 2010, Vedel et al. 2011 DiGirollomo and Dodds 2017
acid (Krčmar et al. 2010), and aged animal urine (Krčmar et al. 2012, Barimani Varandi et al. 2018). However, other studies that
2005, Krčmar et al. 2006, Krčmar et al. 2010, Tunnakundacha et al. used finer taxonomic units found that Malaise traps collect more
2017), as well as the addition of objects that reflect horizontally po- specimens of certain beetle families (e.g., Cleridae, Curculionidae,
larized light, such as large, round, black object like an inflated beach and Elateridae) or certain tribes and genera within a family (e.g.,
ball covered in black cloth (Catts 1970, Schreck et al. 1993, Blahó lebiine carabids) than light, window, and sticky, colored pan, or pit-
2009) increase the number of Tabanidae caught in Malaise and fall traps (Hosking 1979, Skvarla and Dowling 2017).
canopy traps, though some have not reported differences (Leprince Malaise and canopy traps collect fewer Stomoxys Geoffroy,
et al. 1994). 1-octen-3-ol is also attractive to Culicidae (Nilssen 1762 (Diptera: Muscidae) and Tabanidae compared to Vavoua and
1998). 2,4-hexadlenyl butyrate and heptyl butyrate are highly po- Nzi traps, respectively (van Hennekeler et al. 2008, Krčmar 2017,
tent, specific lures attractive to yellowjackets (Vespula Thomson, Tunnakundacha et al. 2017).
Table 6. Target taxa and trapping statistics from publications that reported accumulation or rarefaction curves for Malaise trap collections
A Malaise trap day is one Malaise trap run for one day, such that 10 Malaise trap days can be accomplished by one trap run for 10 d, two traps run for five days each, etc. Publications that reported traps were run for one
year that did not provide specific dates (e.g., June 2018–May 2019) were assumed to be 365 d.
a
After only 1% of trap catch was sorted and identified to species.
Annals of the Entomological Society of America, 2020, Vol. XX, No. XX
higher degree of brachyceran community heterogeneity using β di- Finally, based on the handful of studies that have reported col-
versity’ (Favret et al. 2019). lection or rarefaction curves for Malaise trap collections, it is clear
Malaise traps are able to function in damp conditions so may be that it is extremely difficult to impossible to exhaustively sample
preferable to vacuum-sampling understory vegetation that is con- Malaise trap-collected arthropods in even a relatively small area
stantly wet (Noyes 1989). (Table 6). Those studies that calculated how much additional ef-
Malaise traps and sweep netting can differentially sample re- fort would be required to exhaustively sample their target taxa
lated genera; for example, within Tabanidae the majority of Tabanus reported a 3.9- to 10.5-fold increase in effort. How much effort
and Hybomitra are collected in Malaise traps while the majority of is required is determined by how large an area is being surveyed,
Chrysops are collected by netting (Tallamy et al. 1976, Strickler and how diverse the target taxa are, and how efficiently Malaise traps
Walker 1993). When targeting Ichneumonoidea, Malaise traps are collect them.
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