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Phylogeny, taxonomy and species delimitation
of water mites and velvet mites
Jeanette Stålstedt
Phylogeny, taxonomy and species delimitation
of water mites and velvet mites
Jeanette Stålstedt
Cover picture: Leptus (Parasitengona, Erythraeoidea) on
Öland, Sweden. Photo by Johan Myhrer.
©Jeanette Stålstedt, Stockholm University 2017
ISBN print 978-91-7649-688-6
ISBN PDF 978-91-7649-689-3
Printed in Sweden by US-AB, Stockholm 2017
Distributor: Department of Zoology, Stockholm University
Abstract
This study is part of the Swedish Taxonomy Initiative (STI) - one of the
most ambitious all taxa biodiversity inventories in the world. One of the
pillars in STI is to support taxonomic research on the most neglected
taxonomic groups with the aim to lift the level of knowledge of biodiversity
in the country. There is still a lot to be discovered, especially in the
microscopic world, and this includes mites. Many aspects of mite biology
and diversity are poorly known, such as species richness, abundance,
distribution, lifestyle and behavior of species. Mites inhabit all sorts of
aquatic, terrestrial, arboreal and parasitic habitats, nevertheless even in wellstudied systems mites are often overlooked. Despite being among the
smallest of arthropods, they are of medical and economical importance and
may be very abundant in the ecosystems they inhabit. This thesis focuses on
Parasitengona (Acariformes: Prostigmata), one of the most diverse taxa
among the arachnids. It includes the aquatic Hydrachnidia (water mites) and
the terrestrial Trombidia (e.g. velvet mites, chiggers). A unifying
characteristic of Parasitengona is their complex life cycle of active and
inactive stages, parasitic larvae and predatory deutonymphs and adults. They
typically parasitize and prey on arthropods, except the chiggers which have
vertebrates as hosts. The aim of this thesis is to shed light on the phylogeny
and taxonomy of Parasitengona with emphasis on the Swedish fauna. To
achieve this, mites were collected from different localities throughout the
country between the years 2007-2016. Water mites were sampled with a
hand net. Larvae of terrestrial Parasitengona were collected with sweeping
nets and sorted out from malaise trap samples from the Swedish Malaise
Trap Project. To collect the adults Berlese-Tullgren extractor and pitfall
traps were used as well as hand collecting and sifting with litter reducer. The
material collected abroad was kindly provided through collaboration.
Methods used in the papers included morphometrics, multivariate analyses,
experimental rearing, DNA extraction and sequencing, Bayesian
phylogenetic analyses and molecular species delimitation. In papers I and II,
we combine molecular species delimitation models and morphological data
to resolve taxonomical issues. This integrative taxonomic approach of
combining data resulted in Piona dispersa Sokolow, 1926 as a valid species
and redescriptions, new synonyms and neotypes provided for Erythraeus
phalangoides (De Geer, 1778), E. cinereus (Dugès, 1834) and E. regalis
(C.L. Koch, 1837). Based on the new inventories we produce an updated and
annotated checklist of 105 terrestrial Parasitengona species for Fennoscandia
in paper III, and use metadata to increase the knowledge on distribution,
habitat preferences, life stages and abundance. Out of these, 20 species are
new findings for the region and five are potential new species for science. In
paper IV, we provide a molecular phylogeny of Parasitengona based on the
genes 18S, 28S and COI for 80 taxa with a sampling focus on the terrestrial
lineages. Based on the results we offer a revised higher-level classification
of the group. In particular the analyses supported Tanaupodoidea Thor, 1935
as a separate superfamily, but Trombiculoidea Ewing, 1929 was not
monophyletic and was synonymized, along with Chyzerioidea Womersley,
1954, with Trombidioidea Leach, 1815.
In Swedish:
Studien ingår i ett av de mest ambitiösa projekten i världen för att kartlägga
all biologisk mångfald inom ett område- Svenska artprojektet (STI). En av
hörnstenarna i STI är att stödja taxonomisk forskning på dåligt kända
organismgrupper med syftet att lyfta kunskapsnivån om biologisk mångfald i
landet. Kvalster är en av dessa organismgrupper. De lever i de flesta
akvatiska ochterrestra habitat, samt som parasiter, men de förbises ofta även
i väl studerade ekosystem. Ett flertal arter är av medicinskt och ekonomiskt
intresse och kan utgöra en viktig beståndsdel i de ekosystem de lever. Denna
avhandling fokuserar på Parasitengona (Acariformes: Prostigmata) som
inkluderar vattenkvalster (Hydrachnidia), sammetskvalster och löpkvalster
(Trombidia). Jämförelsevis med övriga kvalster är dessa större i storlek och
färgstarka. Därför kallas de ibland för "jättarna" eller "fjärilarna i
kvalstervärlden". Parasitengona karakteriseras av deras komplicerade
livscykel med alternerande aktiva och inaktiva stadier. Larver är ofta
parasitiska medan aktiva nymfer och adulter är glupska rovdjur. De lever på
leddjur, förutom "chiggers" som har ryggradsdjur som värd. Målet med
avhandlingen var att utforska Parasitengonas fylogeni och taxonomi, med
fokus på den svenska faunan. För att uppnå detta insamlades kvalster på
olika orter runtom i landet mellan åren 2007-2016. Vattenkvalster
insamlades med håv. Larver av terrestra Parasitengona fångades in med
slaghåv och sorterades ut från Svenska Malaisefälleprojektets material. De
vuxna djuren plockades vid förnasortering eller direkt för hand, men även
med hjälp av Berlese-Tullgren trattar och fallfällor. Utländskt material kunde
inkluderas tack vare internationellt samarbete. Morfometri, multivariata
analyser, uppfödning, sekvensering, släktskapsanalyser och molekylära
artavgränsningsmodeller var metoder som användes. I första och andra
artikeln, fokuserar vi särskilt på nyttan av att kombinera molekylära
artavgränsningsmodeller och morfologiska metoder för att lösa taxonomiska
frågor. Denna integrerade metod resulterade i Piona dispersa Sokolow, 1926
som giltig art och ombeskrivningar, nya synonymer och neotyper för
Erythraeus. phalangoides (De Geer, 1778), E. cinereus (Dugès, 1834) och E.
regalis (C.L. Koch, 1837). I tredje artikeln sammanställer vi en checklista
över 105 terrestra Parasitengona arter i Fennoskandien och använder
metadata från insamlingsplatser för att öka kunskapen om arters utbredning,
habitatpreferenser, livsstadier och förekomst. Av dessa är tjugo arter nya för
regionen och fem är potentiellt nya arter för vetenskapen. I fjärde artikeln
presenterar vi en molekylär fylogeni över terrestra Parasitengona baserat på
generna 18S, 28S och COI för 80 taxa. Baserat på resultatet ger vi en
reviderad klassificering för gruppen. Resultaten stödjer Tanaupodoidea Thor,
1935 som överfamilj, men Trombiculoidea Ewing, 1929 var inte
monofyletisk och synomiseras, liksom Chyzerioidea Womersley, 1954, med
Trombidioidea Leach, 1815.
List of papers
The thesis is based on the following articles, which are referred to in the
text by their Roman numerals:
I
Stålstedt, J., Bergsten, J., & Ronquist F. (2013) ”Forms” of
water mites (Acari: Hydrachnidiae): intraspecific variation or
valid species? Ecology and Evolution, 3(10): 3415–3435.
II
Stålstedt, J., Wohltmann, A., Bergsten, J., & Mąkol, J. (2016).
Towards resolving the double classification in Erythraeus
(Actinotrichida: Erythraeidae): matching larvae with adults using
28s sequence data and experimental rearing. Organisms Diversity
& Evolution, 16:761–790.
III
Stålstedt, J., Łaydanowicz, J., Lehtinen, P.T., Bergsten, J. &
Mąkol, J. Checklist of Terrestrial Parasitengona mites
(Acariformes: Prostigmata) in Fennoscandia – Manuscript
intended for Biodiversity Data Journal.
IV
Stålstedt, J., Mąkol, J. Dabert, M., Wohltmann, A., Dabert, J. &
Bergsten, J. Phylogeny and revised classification of terrestrial
Parasitengona –Manuscript.
Papers I and II are open access articles distributed under the terms of
the Creative Commons Attribution License.
The nomenclatural acts in papers III and IV are not issued for
permanent scientific records or for purposes of Zoological
Nomenclature and are not regarded as published within the meaning
of the International Code of Zoological nomenclature (ICZN, ed. 4,
article 8.2).
Candidate contributions to thesis articles*
I
II
III
IV
Conceived the study
Substantial
Substantial
Substantial
Substantial
Designed the study
Substantial
Substantial
Substantial
Significant
Collected the data
Substantial
Significant
Significant
Substantial
Analysed the data
Substantial
Substantial
Substantial
Substantial
Manuscript preparation
Substantial
Significant
Substantial
Significant
* Contribution Explanation
Minor: contributed in some way, but contribution was limited.
Significant: provided a significant contribution to the work.
Substantial: took the lead role and performed the majority of the work.
Contents
Introduction .................................................................................................... 13
Linnaeus’ work continues ......................................................................................... 13
What is a Parasitengona mite? ................................................................................... 14
Evolution of Parasitengona ........................................................................................ 17
Aim of the thesis ...................................................................................................... 18
Material and methods ....................................................................................... 19
Collected material .................................................................................................... 19
Morphometrics ........................................................................................................ 20
Multivariate analyses ................................................................................................ 20
Rearing ................................................................................................................... 20
Gene trees ............................................................................................................... 21
Species delimitation models ...................................................................................... 21
Summary of papers .......................................................................................... 22
Paper I .................................................................................................................... 22
Paper II ................................................................................................................... 23
Paper III .................................................................................................................. 24
Paper IV.................................................................................................................. 24
Discussion ...................................................................................................... 25
Acknowledgements .......................................................................................... 27
References ...................................................................................................... 29
Introduction
Linnaeus’ work continues
Acarology probably started 35 BC with Aristotle, who named the tiny
animal akari and which Linnaeus in 1758 latinized to Acarus. It wasn’t until
the late 1800s that the term “acarologist” arose to describe those who study
mites and in the middle of the 1900s the word started to appear in
dictionaries (Krantz 1996). In Linnaeus’s Systema Naturae 31 species were
included (Linnaeus 1758). This inspired a large number of biologists to start
something amazing, namely the discovery of biodiversity in poorly known
groups. Early works of acarology were performed by Koch, Dugés, Berlese,
Kramer, Grandjean, to name only a few. Today, approximately 55,000
species are described (Zhang et al. 2011; Walter & Proctor 2013). However,
this probably represents only 5% of the real fauna. Although not equal to
insects, mites do rank high in species richness (Walter & Proctor 2013).The
biodiversity and biology of mites, in aspect of species richness, abundance,
lifestyle and behavior of the species, are poorly known in general. Mites
inhabits all sorts of aquatic, terrestrial, arboreal and parasitic habitats,
nevertheless even in well-studied systems mites are often overlooked.
Despite being among the smallest of arthropods, they are highly active in the
ecosystem as parasites on animals and plants, detritivores, predators or a
combination of several feeding behaviors (Walter & Proctor 2013). They can
be adaptable in bodysize which can result in successful exploitation of
microhabitats. This also demands microscope equipment, which is essential
for identification. The range of size is relatively wide when comparing the
largest and smallest of mites. Giant red velvet mites can become almost 2 cm
in length, while gall mites can be as short as 80 μm (Lindquist et al. 1996).
Linnaeus’ vision of mapping all life has so far not been achieved, not even in
his home country of Sweden. Today, a large scale project called the Swedish
Taxonomy Initiative, financed by the Swedish government, is continuing his
work. The goal is to identify all species of multicellular plants, fungi and
animals in the country. There is still a lot to be discovered, especially in the
microscopic world. Naturally, this includes mites. In Sweden we have over
1,000 species of Acari known (Gärdenfors et al. 2003). Most of these are
represented in the collections at the Zoology Museum in Lund and the
Swedish Museum of Natural History in Stockholm. Moss mites (Oridatida)
13
and water mites (aquatic Parasitengona , Hydrachnidia) have been studied
the most. After Linnaeus and De Geers work, Carl Herman W. Andersén
(1863) raises the knowledge from 21 to 137 Swedish species (Bock 2017).
Ivar Trägårdh, Karl-Herman Forsslund, Per Dalenius and Nils TarrasWahlberg have published papers with emphasis on moss mites, and moss
mites in forest ecosystem have been studied by the Swedish University of
Agricultural Sciences in Uppsala (Lundqvist 1987). One of the first papers
on Swedish water mite fauna was published by Carl Julius Neuman with 72
species recognized (Neuman 1880). In 1927, 1962 and 1968, Olov Lundblad
published his major findings in “Die Hydracarinen Schwedens”, in three
parts. For each of the 235 species recognized with detailed location data, he
produced a series of perfect slide preparations. However, a number of
morphological variants called “forms” were a taxonomical challenge. Did
these morphotypes represent intra- or interspecific variation? Morphological
and genetic data imply that the forms are separate species and therefore the
majority of them are considered valid in Fauna Europaea (Davids &
Kouwets 1987; Gerecke 2014; Stålstedt et al. 2013). Today, 252 Swedish
species are recorded (Lundblad 1962; Böttger & Ullrich 1974; Nordqvist &
Herrmann 2008; Dyntaxa 2013; Stålstedt et al. 2013; Stålstedt unpublished).
In contrast, the Swedish fauna of terrestrial Parasitengona (Trombidia) was
very poorly known. Gärdenfors et al. (2003) listed 12 species. With
literature and collections thoroughly searched and recent findings added
(Haitlinger 2008), we summarized it to about 30 species at the start of this
project with the help of Lars Lundqvist (Zoology Museum in Lund). To date,
47 Swedish species are known (Stålstedt et al. unpublished; paper III).
Species were mostly described based on adults in the early years, but have
more commonly been described as larvae in the last decades (Wohltmann
2000; Zhang & Fan 2007). Because of the difficulty of matching the
heteromorphic larval and post-larval stages, this has created a problem with
“double classification”. This means that the actual number of species in
Europe may be anywhere between 300 and 500 out of the 680 nominal
species of terrestrial Parasitengona (Mąkol & Wohltmann 2012, 2013; paper
II).
What is a Parasitengona mite?
Parasitengona is made up of two ecologically distinct assemblages, the
aquatic Hydrachnidia and the terrestrial Trombidia. Relative to the
remaining mites, these are larger in size and more colorful. Therefore they
are sometimes called “the giants” or “the butterflies of the Acari world”. The
most striking appearance is the intensely red color, but they can also be
purple, orange, yellow, blue, green and brown. The terrestrial Trombidia and
in particular its superfamily Trombidioidea are called “velvet mites”. This is
14
due to the red color and “furry” appearance by numerous setae, of its most
famous family Trombidiidae (Proctor 1998). This family is sometimes called
“true velvet mites” or “red velvet mites”. “Chiggers” or “scrub itch mites”
(Trombiculidae) parasitize on vertebrate hosts and can act as vector for
several diseases (paper IV). “Water mites” (Hydrachnidia) have also been
referred as Hydrachnidiae, Hydrachnida, Hydracarina or Hydrachnellae,
while the two latter names are no longer used. In the past, limnic species of
Halacaridae (Prostigmata) were wrongly included (Di Sabatino et al. 2000).
The Parasitengona (Acariformes: Prostigmata) constitute one of the most
diverse taxa among the arachnids. There are over 11,000 known species of
Parasitengona (Walter & Proctor 2013). This number is considered a great
underestimate of the true species diversity, since Africa, Asia, and South
America have been poorly studied to date (Smith & Cook 1991; Di Sabatino
et al. 2000). It is estimated that water mites alone would reasonably be more
than 10,000 species (Di Sabatino et al. 2008). By recent classifications, they
are grouped into either fourteen (Krantz & Walter 2009), seventeen (Zhang
et al. 2011) or eleven superfamilies (Davids et al. 2007; Mąkol &
Wohltmann 2012, 2013). The lack of consensus mostly affects the
composition of Trombidioidea and it is mainly due to the fact that no well
supported phylogeny of terrestrial Parasitengona exists.
A unifying characteristic of Parasitengona is their complex life cycle
consisting of a parasitic larva, two inactive pupa-like calyptostatic stages that
represent the protonymph and tritonymph, and active predatory
deutonymphal and adult stages. The larvae usually parasitize on arthropods
while the active postlarval stages (deutonymph and adult) are predators. The
deutonymph is similar to the adult, but adults have a genital opening for
reproduction and they are often more developed in size and other characters.
In contrast to being the most common host for water mites, Chironomidae is
rarely parasitized by terrestrial larvae. But Tipulidae represents a group used
as host for both Trombidia and Hydrachnidia. Terrestrial Parasitengona prey
mostly on insect eggs and larvae, but species predation on insect imagines
and mites have been observed (Wohltmann et al. 2007). Water mites
contribute in regulating mosquito populations, especially in habitats were
fish is absent (Di Sabatino et al. 2000; Davids et al. 2007). However, small
crustaceans are also an important food source for water mites (Proctor &
Pritchard 1989). They have been proposed as suitable bioindicators due to
their dependence on host and prey, sensitivity to altered sediment structure
and poor water quality influenced by organic waste, heavy metals or other
poisonous compounds (Goldschmidt 2016).
Trombidioidea are abundant both in woodland areas and in open habitats
(Wohltmann 2000). They often burrow themselves and some only emerge to
15
the soil surface for mating. They can be found in soil, humus, moss, litter or
sand, ranging from xeric to hygric habitats (Zhang 1998). Major taxonomic
and phylogenetic revisions are needed in nearly all taxa (Zhang 1998;
Wohltmann 2000). Nevertheless, some groups have been treated in the
relatively recent literature. Revision has been made by Southcott on
Trombidiidae (1986), Johnstonianidae (1987), Eutrombidiidae (1993) and
Microtrombidiidae (1994). A revision of postlarval Microtrombidiidae was
published by Gabryś (1996; 1999). Mąkol (2007) revised Trombidiidae and
Podothrombiidae, and Wohltmann et al. (2004) revised European
Johnstonianidae. In contrast to Trombidioidea, Erythraeoidea contains many
fast-moving and long-legged species. They are mostly found in open and dry
landscapes but some species occur in hygric habitats and its calyptostatic
stages can survive flooding. They live in or on the litter layer, but can also be
found hiding under bark of trees and under rocks. Larvae can attach to hosts,
even fast moving ones, with the help of a sticky secretion. Balaustium von
Heyden, 1826 and some Abrolophus Berlese, 1891 species have predatory
larvae (Wohltmann et al. 2007). Calyptostomatoidea and Tanaupodoidea
contain solely one single family each. Tanaupodoidea occur in moist litter
and Calyptostomatoidea mostly in wet or moist litter and moss habitats
(Krantz & Walter 2009). In Europe, Calyptostomatoidea is represented by a
single species, Calyptostoma velutinus (Müller, 1776). However, it is
suggested that this taxon represent more than one species (Wohltmann et al.
1999; paper III).
Water mites are often classified into eight superfamilies. They live in lakes,
temporary waters, streams and springs. The calyptostatic stages give an
advantage in avoiding drought and the larval parasitism opens up for rapid
and long-distance dispersal on flying insects (Di Sabatino et al. 2002). The
Hydryphantoidea, Eylaoidea and Hydrachnoidea are mostly red and
relatively large sized, while Lebertioidea, Hygrobatoidea, Arrenuroidea
often have a combination of green, brown, yellow, red and blue coloration
(Di Sabatino et al. 2002; Krantz & Walter 2009; Di Sabatino et al. 2010).
Body-shapes are also highly variable. For instance, Oxidae within
Lebertioidea are flattened laterally. Hydrovolzioidea, composed of two small
families, have highly distinctive, sclerotized and dorso-ventrally flattened
bodies and some morphological similarity to Halacaroidea (Prostigmata) (Di
Sabatino et al. 2010). Stygothrombioidea with its single genus have
elongated (worm-like) bodies and seems to occur interstitially burrowed in
the bottom sediment in lotic habitats (Krantz & Walter 2009). Arrenuroidea
are mostly sclerotized mites and consists of twenty families, and the genus
Arrenurus Duges, 1834 is known to prefer Odonata as host (Krantz & Walter
2009; Zhang et al. 2011). Adults of a few species of Hygrobatoidea live in
the mantle cavity of molluscs or in the canal system of sponges.
16
Evolution of Parasitengona
Although the relation among the arachnid lineages is uncertain, molecular
phylogenies indicate that Acari is paraphyletic, comprising the two
superorders Acariformes and Parasitiformes. Parasitengona belong to the
very diverse order of Trombidiformes within Acariformes. The phylogenetic
relationships within Parasitengona are uncertain. It seems that water mites is
not a sister group but nested within the terrestrial Trombidia but with an
uncertain placement (Welbourn 1991; Dabert et al. 2010, 2016; paper IV)
(Fig. 1). The molecular data suggest Stygothrombioidea or
Calyptostomatoidea as the closest relative of water mites (Dabert et al.
2016). Although originally considered a polyphyletic assemblage of waterliving forms, the consensus now is that Hydrachnidia forms a monophyletic
group at least without Stygothrombioidea (Dabert et al. 2016). Keeping the
superfamily Hydrovolzioidea within Hydrachnidia, was confirmed with the
help of scanning electron microscope and molecular data (Alberti & Bader
1990; Dabert et al. 2016). The Stygothrombioidea however, is harder to
place. It is unclear if Stygothrombioidea represenst an independent invasion
of freshwater or if they belong to the water mites as a superfamily within
Hydrachnidia (Wohltmann et al. 2007; Krantz & Walter 2009; Walter &
Proctor 2013; Dabert et al. 2016). They have the two defining characters of
water mites (two setae on larval palpal genu and presence of glandularia)
that are lacking in terrestrial Parasitengona. However, they also have
trichobothria and well-developed empodial claw in the adult, which is absent
in Hydrachnidia (Walter & Proctor 2013).
A
Erythraeoidea
Calyptostomatoidea
Hydrachnidia (Water mites)
Stygothrombioidea
Hydrachnidia (Water mites)
Calyptostomatoidea
Tanaupodoidea
Erythraeoidea
Chyzerioidea
Trombiculoidea
Trombiculoidea
Chyzerioidea
Trombidioidea
Trombidioidea
Parasitengona
?
B
Figure 1. Phylogenetic relationship among major lineages of Parasitengona based
on (A) the morphological data by Welbourn (1991) and (B) the molecular data by
Dabert et al. (2016).
17
Aim of the thesis
The aim of this thesis is to shed light on the phylogeny and taxonomy of
Parasitengona with emphasis on the Swedish fauna. To achieve this, I
specifially focused on:
¾ The utility of combining molecular species delimitation models and
morphological methods to resolve taxonomical issues, such as the status
of morphological forms (paper I) and matching heteromorphic larvae
with adults (paper II).
¾ Identifying the fauna of terrestrial Parasitengona in Fennoscandia by
new collecting efforts and using metadata from inventories to give
additional insight into the habitat preferences, phenology of life stages,
distribution and abundance of species (paper III).
¾ Reconstruct a molecular phylogeny of Parasitengona based on multiple
genes and a taxon-sampling focus on the terrestrial lineages, and from
this produce a revised higher-level classification (paper IV).
18
Material and methods
Collected material
Inventory in Sweden, was done between the years 2007-2016 on different
localities throughout the country. The largest sampling effort was conducted
in 2008 and 2013. Water mites were sampled with a hand net (mesh size 0.5
mm) and the living material was sorted in the laboratory or directly in the
field. In paper I, running and standing water in the provinces of Uppland
and Småland in Sweden were chosen on the basis of earlier findings of
Lundblad (1962; 1968). Most of the larval material of terrestrial mites was
kindly provided by the Swedish Malaise Trap Project (SMTP) (paper II, III
and paper IV). SMTP is a remarkable three-year inventory (2003-2006) of
the Swedish insect fauna using over 70 Malaise traps placed around the
country and maintained by volunteers (Karlsson et al. 2005). The sorting of
Acari (without or with hosts) was done by SMTP at Station Linné on Öland
and further sorting of Prostigmata and Parasitengona was done at the
Swedish Museum of Natural History. The adults were collected by sifting
(litter reducer) or hand picking in the field. Hand net (larvae), BerleseTullgren apparatus and pitfall traps were also used. Localities for collecting
terrestrial adults were selected based on relative quantities of larvae
(parasiting on winged insects) sorted from different SMTP-traps (paper II,
III and paper IV). In many cases, the adults were found active in the litter
surface and close to water habitats. In June 2013, I had help with the
collecting from Rasmus Hovmöller (Swedish Museum of Natural History)
who was at that time field assistant in the project and Magdalena Felska
(Wroclaw University of Environmental and Life Sciences), who at that time
was a PhD student in Poland. Better understanding about collection methods
and habitat preferences were kindly taught in the field by her. All Swedish
material studied for this thesis is either stored in ethanol (80%, -20°C) or
mounted on slides (euparal mounting media). Swedish material and DNA
extractions are deposited at the Swedish Museum of Natural History
(NHRS). In paper III, species occurrence records of terrestrial mites in
Fennoscandia are documented by georeferenced locality data and additional
metadata. Data from Norway and Finland was provided by Joanna Mąkol,
Joanna Łaydanowicz and Pekka T. Lehtinen. Mites collected abroad for
DNA extraction in paper IV was loaned to me by Joanna Mąkol, Andreas
Wohltmann, Cal Welbourn and Hans Klompen. Additional specimens were
19
provided by Johannes Bergsten. Sequences were provided by J. Dabert, M.
Dabert and Genbank. The remaining material was collected in Sweden.
Morphometrics
Measurements were taken with a Leitz Wetzlar Laborlux S microscope
(paper I) and Nikon Eclipse 80i (paper II, III, IV). Aquatic Parasitengona
were identified with the help of Viets (1936), Lundblad (1962; 1968) Davids
et al. (2007) and Di Sabatino et al. (2010), while terrestrial Parasitengona
were identified using Haitlinger (1987; 2003) and Wohltmann et al. (2007).
Identification in paper II of Erythraeus species was challenging and needed
comparisons with a reference collection of Palearctic species (coll. Joanna
Mąkol, Wrocław University of Environmental and Life Sciences, Poland).
Important morphological characters in Piona and Unionicola are palps,
genital acetabula and, if present, claw of the males’ third leg.In Erythraeus
palpal conalae, setae (body and legs, often modified) and crista metopica are
the most important characters. Qualitative characters are of special
importance (e.g. shape), while in Erythraeus larvae quantitative
measurements are also required. All measurements are taken with an ocular
micrometer. The total length of legs includes coxae. Terminology,
abbreviations applied to morphological structures, and measurement
standards follow Wohltmann et al. (2007) and Mąkol (2010).
Multivariate analyses
Characters of males and females for each genus were analyzed separately in
a principal component analyses performed in R version 2.8.1 (R
Development Core Team 2008). Measurements were taken of the width and
length of the body, fourth coxa (in Unionicola specimens the fused coxa III
and IV), palpal femur (P-II), and palpal tibia (P-IV).We also measured the
dorsal length of the remaining segments of the palp. In addition, we counted
the sclerotized and unsclerotized genital acetabula of females, and measured
the width and length of the tarsus and claw of the males’ third leg.
Rearing
Experimental rearing was performed by Andreas Wohltmann and Joanna
Mąkol. Larvae were obtained from field-collected females. The diapausing
life stage of each particular species was recognized. The material was kept at
controlled temperature (20 °C, ±1 °C tolerance) and light (12 h dark, 12 h
light) in environmental chambers. In case of successful development of eggs
into larvae, the recorded rearing success was >90 %. When development
stopped at a certain instar, specimens were exposed to 5 °C for about 90 days
and subsequently re-exposed to 20 °C in order to imitate winter conditions
20
and to break diapause. Test on the influence of humidity followed
procedures described in Wohltmann (1998). Host and food were offered.
Gene trees
The molecular work was carried out at the Molecular Systematics
Laboratory (MSL), Swedish Museum of Natural History. DNA was
extracted from the tissue of four legs of each individual or the whole mite,
depending on size. For the molecular analyses, DNA was extracted and
sequenced using standard protocols. Three genes were used, one
mitochondrial (COI) and two nuclear genes (18S and 28S). DNA sequences
were aligned using MAFFT or ClustalW (Katoh et al. 2005; Larkin et al.
2007). The third codon position of COI and some of the highly variable and
poorly aligned regions of 18S and 28S were excluded for the higher-level
phylogeny. Regions were identified using Gblocks v.0.91b (Castresana
2000). Phylogenetic trees were reconstructed with Bayesian methods, using
MrBayes (Ronquist & Huelsenbeck 2003; Ronquist et al. 2012) and BEAST
(Bouckaert et al. 2014). Nucleotide composition statistics, genetic intra- and
interspecific distances (Kimura 1980), and parsimony informative characters
were obtained using MEGA (Tamura et al. 2013).
Species delimitation models
Molecular species delimitation was conducted using the generalized mixed
Yule-coalescent model (GMYC) in paper I and paper II (Pons et al. 2006;
Fujisawa & Barraclough 2013), Rosenberg’s (2007) test of reciprocal
monophyly and Rodrigo et al.’s (2008) test of branch length ratios. These
are all tested with single-locus gene trees. The GMYC analysis was
performed in R with the “splits” package (Ezard et al. 2014; R Core Team
2015).
21
Summary of papers
Paper I
Stålstedt, J., Bergsten, J., & Ronquist F. (2013) ”Forms” of water mites
(Acari: Hydrachnidiae): intraspecific variation or valid species? Ecology and
Evolution, 3(10): 3415–3435.
In many groups of organisms, especially in the older literature, it has been
common practice to recognize sympatrically occurring phenotypic variants
of a species as "forms". In this study, we test a number of what is now
recognized as valid species of water mites, but which have in the past been
treated as forms. A form currently not recognized as a valid species, was also
tested. The molecular species delimitation models, mitochondrial COI,
nuclear 28S and quantitative analyses of morphological data supported that
all forms are separately evolving lineages. The genetic distance between the
form Piona dispersa Sokolow, 1926 and the nominate species Piona
variabilis (Koch, 1836) was 11%. We propose that P. dispersa are
recognized as a valid taxon at the species level. The DNA data also revealed
that some taxa likely represent more than one species.
Female of Unionicola minor (Soar, 1900).
22
Paper III
Stålstedt, J., Łaydanowicz, J., Lehtinen, P.T., Bergsten, J. & Mąkol, J.
Checklist of Terrestrial Parasitengona mites (Acariformes: Prostigmata) in
Fennoscandia – Manuscript intended for Biodiversity Data Journal.
The knowledge of terrestrial Parasitengona in Fennoscandia lags far behind
that of the aquatic counterpart, the water mites (Hydrachnidia). Based on
new inventories we provide primary data and an annotated checklist of
terrestrial Parasitengona in Fennoscandia including 110 species. Out of
these, 20 species are new findings for the region and five are potential new
species for science. 19 species were new for Norway, 15 for Finland and 8
for Sweden. The known recorded fauna today of terrestrial Parasitengona is
73 species for Norway, 47 for Sweden and 47 for Finland. Primary data
include georeferenced locality data as well as collecting techniques and
microhabitat to increase the knowledge on species’ habitat requirements.
The higher recorded diversity for Norway is likely the result of a relatively
larger effort.
Paper IV
Stålstedt, J., Mąkol, J., Dabert, M., Wohltmann, A., Dabert, J. & Bergsten, J.
Phylogeny and revised classification of terrestrial Parasitengona –
Manuscript.
The phylogenetic relationship between Hydrachnidia and Trombidia has
been debated and the molecular phylogeny of Hydrachnidia was recently
tested. Here we provide and analyze the most comprehensive molecular
dataset of terrestrial Parasitengones to date based on the genes 18S, 28S and
COI for 80 taxa. Hydrachnidia is nested within Trombidia and sister group to
Calyptostomatoidea. Stygothrombioidea is sister to remaining Parasitengona,
Erythraeoidea and Tanaupodoidea are sister taxa and Trombiculoidea is a
paraphyletic clade along with Chyzerioidea in relation to Trombidioidea.
Based on the result we recognize five non-Hydrachnidia superfamilies:
Stygothrombioidea Thor, 1935, Tanaupodoidea Thor, 1935,
Calyptostomatoidea Oudemans, 1923, Erythraeoidea Robineau-Desvoidy,
1828 and Trombidioidea Leach, 1815 (=Trombiculoidea Ewing, 1929 (n.
syn.); =Chyzerioidea Womersley, 1954 (n. syn.); =Yurebilloidea Southcott,
1996) (n. syn.)). We also suggest Podothrombiidae Thor, 1935 to be valid at
family level (n. stat.).
24
Discussion
The limit of a species is not always easy to determine and depends on the
species concept used. In papers I and II we use the unified species concept
(DeQuieroz, 2007). In the case of Unionicola crassipes – U. minor complex
(Hygrobatoidea) we concluded that until further data becomes available, U.
minor should not to be delimited into four separated species as showed by
the molecular analyses. De Quieroz (2007) suggested that preferably
multiple lines of evidence should be available to support that two taxa are
separately evolving. The multivariate analysis did not find a character
supporting this and we were not able to reject that the variation in palp shape
was continuous. Unionicola crassipes and U. minor on the other hand have
relatively discrete morphological characters, different behavior and
molecular support and can by the unified species concept be considered
separate species. In paper I and II we used molecular species delimitation
models together with morphological evidence to solve taxonomical
questions and state the importance of combining molecular and
morphological methods. The experimental rearing did not only support the
molecular delimitation but additionally gave more biological data on the life
stages which could not be obtained solely by molecular data. In addition to
the three Erythraeus species in paper II, material is already available for
four new redescriptions of Erythraeus spp.
To date, 299 Swedish species of Parasitengona are known (Stålstedt
unpublished; paper III). In comparison to water mites in neighboring
countries, 158 species in Norway (Mehl 1979; Stålstedt unpublished) and
139 in Finland (Bagge & Bagge 2009), Sweden is well studied with its 252
species. Despite this, there are still areas of biological interest in Sweden that
have not been surveyed. The fauna of the remaining Nordic countries is yet
to be well explored even if Finland and Norway is not expected to be as
diverse as Sweden. Regarding the terrestrial Parasitengona, a Norwegian
inventory was conducted by Joanna Łaydanowicz, a former PhD student at
Wrocław University of Environmental and Life Sciences in Poland. Despite
limited in geographic area, the sampling was thorough in terms of
microhabitats. With Norway’s 73 species and northern localities still to be
explored the actual number of species can be higher (paper III). In Finland,
the collection area was even more limited to the southern parts. The
25
sampling effort made in Sweden was quite comprehensive and resulted in
sorted material which is still being processed.
The phylogeny in paper IV while being the most comprehensive to date,
shows the need for additional genes and taxa for a better resolution in future
analyses. Especially the lacking families Walchiidae, Leeuwenhoekiidae,
Neotrombidiidae, Audyanidae, Yurebillidae, Achaemenothrombiidae,
Amphotrombiidae and Allotanaupodidae should be included in the future.
Additional representatives of Tanaupodidae, Trombellidae, Chyzeriidae and
Neothrombiidae are also needed. Geographically, the Asian and Africa
continent was poorly represented in this study. At the same time, it is clear
that to resolve the backbone of Parasitengona the three genes 18S, 28S and
COI is not enough, and future studies should aim for more nuclear genes.
It has been fifteen years since the Swedish Taxonomy Initiative (STI) was
established and more than 3,000 species have been discovered as new for the
Swedish flora and fauna since then. From this thesis ten more species can be
added to that list, plus two potential new species for science. For sure there
are more to be found in the diverse group of mites. In Parasitengona mites
alone, it is reasonable to assume that the Swedish fauna is at least as diverse
as what is now known from Norway which would mean more than twenty
species remain to be discovered. In addition, fourteen taxa have been raised
to species level since Lundblad’s (1968) studies and about twenty records
rediscovered in the literature since Gärdenfors et al. (2003). However, old
literature records can also be based on misidentifications or in some cases be
from habitats that no longer exist where they used to. Therefore it is
necessary that the findings can be confirmed with recent studies. Molecular
data open up possibilities for new research and surely mite systematics will
gain from this. I hope this thesis is a step on the way towards an improved
classification of Parasitengona and charting of its biodiversity. Hopefully
this thesis contributes to the knowledge of this poorly known
organismgroup, in line with STI’s and Linnaeus’ vision on naming and
knowing the biodiversity in Sweden and globally.
26
Acknowledgements
This PhD study is financed by the Swedish Taxonomy Initiative (The
Swedish Species Information Centre) and I am very grateful for the support.
Stipendia was given by Riksmusei Vänner and Entomologiska
Föreningen i Stockholm for traveling to Japan and Poland. I also appreciate
the financial support by Biofokus (Oslo, Norway) and Artningshjälpen
(Vindeln, Sweden) for identification of water mites.
I am very grateful for my supervisors’ hard work. Thank you Johannes
Bergsten for being a great supervisor and teaching me molecular
delimitation models, recent systematic strategies in arthropods through the
journal club sessions and the importance of the written word to make your
research available to science, not only for those working on the taxonomic
group but for all interested in systematics. Joanna Mąkol, I am very
impressed by your knowledge and research with terrestrial Parasitengona. I
would like to thank you for teaching me the identification, terminology,
morphological structures of setae and literature. I also appreciate our field
trip with your students, in the mountains near the border of Czech Republic.
I also want to thank Fredrik Ronquist for his initiative, supervision on the
water mite study and teaching me the basis of molecular phylogeny and
MrBayes.
I want to express my gratitude to my coauthor and independent researcher
Andreas Wohltmann who greatly improved the study of Erythraeus with
his fantastic work on experimental rearing and his contribution on the
phylogeny of terrestrial Parasitengona. I would also like to acknowledge my
coauthors Mirka Dabert and Jacek Dabert for kindly collaborating with us
and improving the phylogenetic study. Additional thanks goes to coauthors
Joanna Łaydanowicz and Pekka T. Lehtinen who provided extensive
locality data for the checklist.
Thank you Magdalena Felska (Wrocław University of Environmental and
Life Sciences, Poland) for visiting me two weeks in the field, making the
terrestrial collecting effort a success. Thanks goes to Rasmus Hovmöller
(NRM) for working as an assistant for four weeks in the field and collecting
mites from Abisko and Vindelfjällen in the north of Sweden.
27
I am also grateful for the material and support given by the staff at the
Swedish Museum of Natural History (NRM). The research and care of the
collections at the Department of Zoology are of great inspiration. I would
like to thank all my colleagues and the head of the department Kjell Arne
Johanson. The staff of the Molecular Systematics Laboratory (MSL, NRM)
is acknowledged for their valuable advice on sequencing, especially the help
from Bodil Cronholm, Martin Irestedt and Keyvan Mirbakhsh. I
appreciate Rasa Bukontaite, Marianne Espeland, Sibylle Häggqvist,
Tobias Malm, Julia Stigenberg, Jonas Strandberg and Emma Wahlberg
who were at the time PhD students at NRM, for their advice on molecular
and morphological analysis. Extra support was given by Rasa and Jonas.
You encourage me to make my best – Thank you!
I would also like to take this opportunity to give my appreciation to Ulf
Lettevall (Växjö) for teaching me water mites when I was Jan Herrmann’s
student at Kalmar University. Thanks are also given to Lars Lundqvist
(Zoology Museum, Lund) and the teachers at the Acarology Summer
Program (Ohio, USA) for teaching me the basics of acarology.
Special thanks to my husband Alexander Stålstedt, for combining mite
sampling with family trips, as well as rereading manuscripts. You are a great
chauffeur! Thanks also goes to my kids, who never complain and enjoy
following me around Sweden.
Collecting mites in the Swedish mountains. Photo by Alexander Stålstedt.
28
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