ChapterPDF Available

Abstract and Figures

Spiders with around 48,000 recorded species are major terrestrial predators and thus crucially important for ecosystem functioning. They are widely used as research models and for biodiversity displays and sometimes also kept as pets. Nevertheless, we are not aware of any legal ethical rules bound to spider welfare during rearing or research. To set ethical standards, we first need to detect and assess how spiders “perceive” the external world. Based on the current knowledge of spiders’ sensory and nervous system, it is difficult to judge whether spiders feel pain, distress and suffering, although their behaviours like thanatosis, “bailing out”, autotomy and associative avoidance learning imply so. As is now known, arthropods are not simply mini-robots as traditionally believed. Thus, spider welfare deserves more research effort, and the ethical standards for rearing or using spiders in research need to be set. Here, we describe the variety of spider physiological and behavioural characteristics and how they apply to their rearing, housing, handling and experimental use. We hope reporting these methods will help ensuring welfare and well-being of spiders in captivity.
Content may be subject to copyright.
Chapter 5
Spider Welfare
Simona Kralj-Fišer and MatjažGregorič
Abstract Spiders with around 48,000 recorded species are major terrestrial preda-
tors and thus crucially important for ecosystem functioning. They are widely used as
research models and for biodiversity displays and sometimes also kept as pets.
Nevertheless, we are not aware of any legal ethical rules bound to spider welfare
during rearing or research. To set ethical standards, we rst need to detect and assess
how spiders perceivethe external world. Based on the current knowledge of
spiderssensory and nervous system, it is difcult to judge whether spiders feel
pain, distress and suffering, although their behaviours like thanatosis, bailing out,
autotomy and associative avoidance learning imply so. As is now known, arthropods
are not simply mini-robots as traditionally believed. Thus, spider welfare deserves
more research effort, and the ethical standards for rearing or using spiders in research
need to be set. Here, we describe the variety of spider physiological and behavioural
characteristics and how they apply to their rearing, housing, handling and experi-
mental use. We hope reporting these methods will help ensuring welfare and well-
being of spiders in captivity.
5.1 Introduction
Spiders (order Araneae, class Arachnida) are one of the most diverse animal groups
on the planet, currently with more than 48,000 described species (World Spider
Catalog 2018). They rank seventh in global diversity, only surpassed by mites and
ticks (Acari) among arachnids (Coddington and Levi 1991). Spiders have occupied
all terrestrial ecosystems (Foelix 2011), are the most important predators in prey
biomass consumption (Nyffeler and Birkhofer 2017) and thus have a crucial role in
ecosystem functioning. Among their most characteristic features are hunting using
venom and the production of silk, natures toughest bre (Foelix 2011). For
millennia, spiders have been a part of human imagination, mythology and art,
S. Kralj-Fišer · M. Gregorič(*)
Institute of Biology, Scientic Research Centre of the Slovenian Academy of Sciences and Arts,
Ljubljana, Slovenia
©Springer Nature Switzerland AG 2019
C. Carere, J. Mather (eds.), The Welfare of Invertebrate Animals, Animal Welfare 18,
symbolizing patience, mischief and malice. They are widely used as research models
in diverse elds, for biodiversity displays, and sometimes also kept as pets. Yet,
arthropods including spiders are traditionally considered mini-robots that lack ex-
ibility (Herberstein 2011). Consequently, professional standards securing spider
welfare in captivity are not clearly established.
To set such standards, we should rst address issues of the ability of spiders to
feel pain, distress and suffering. In the aim of comprehending the inner worldof
spiders, we describe below their sensory and notably complex nervous systems,
which are needed to receive and perceive external stimuli. While spiders lack higher
nerve centres and thus should only be capable of reexive behavioural responses to
dangerous stimuli (nociception), their behavioural and physiological responses
imply their potential to feel pain and stress. Spiders, for example, exhibit behaviours
like thanatosis, bailing outand autotomy when in danger. The results of several
studies further imply that spiders thereby activate their stress (octopamine) system
(Punzo and Punzo 2001; Jones et al. 2011). Several species are also able to modify
their behaviour depending on their previous experiences and exhibit associative
avoidance learning in response to previous experiences with predators.
There is thus plenty of evidence that invertebrates, including spiders, are not just
instinct driven and inexible in their behaviour; rather they show behavioural
plasticity and cognitive abilities, such as attentional priming and memory (Jakob
et al. 2011). This evidence should not be ignored and needs to be used while
establishing the guidelines for securing their welfare. The responsibilities of
researchers to take care for study animals include the experimental procedures and
also providing suitable conditions at which spiders are bred or kept when not being
studied. To maximize welfare, the housing of spiders should incorporate as many of
the important natural living conditions as possible. Also, some research elds can
hardly avoid sacricing individuals. Many scientists use ethanol, freezing or CO
a method of spider euthanasia, but it is has not been tested whether these methods
indeed induce analgesia. Yet the instant death at 60 C might be more humane than
several minutes long drowning in ethanolthe method still widely used in research.
In the following chapter, we aim at presenting an overview of welfare considerations
when keeping and experimenting on spiders in the laboratory.
5.2 Sensory and Nervous System
The spidersmain sensory organs are eyes, lyriform organs, trichobothria and
chemosensory organs (Barth 2013). The sensitivity and distribution of the sensory
organs vary among taxa and largely reect a spiders life style. For example, the
visual ability is much better developed in cursorial spiders compared to
web-building spiders, which mainly rely on their vibratory senses. While most
web-building spiders can only detect the direction of light and motion, cursorial
spiders are capable of forming images. Jumping spiders have exceptional eye sight
adapted for colour vision and high spatial acuity (Blest et al. 1981).
106 S. Kralj-Fišer and M. Gregorič
The mechanical senses of spiders involve the specialized hairstrichobothria and
slit sensillae (slits in the exoskeleton) that detect acoustic, vibratory and tactile cues.
Vibratory cues transmitted through environmental surfaces, including silk threads,
are among the most important information sources for spiders. Vibrations inform
them about the presence of prey, mates, parasites and predators. Furthermore,
spiders commonly use vibrations as an intraspecies communication channel, which
is particularly important in mate recognition and mate assessment (Uetz and Roberts
2002). Trichobothria that detect airborne vibrations cover the legs and pedipalps, slit
sensillae that detect substrate-borne vibration are distributed over most of the body
surface, and are most common on legs (Barth 2013). Legs and pedipalps are also
covered by chemosensitive hairs enabling them to recognize conspecics, prey and
predators. Besides the sensory functions of thousands of innervated hairs covering
the spider body, some serve other functions, such as adhesion to the substrate,
combing out silk and cleaning (Foelix 2011).
Sensory organs are innervated. Their axons form small bundles and join into
sensory nerves that conduct the sensory information to the central nervous system
(CNS). The CNS of spiders is highly compacted and consists of two ganglia with
exiting efferent nerves. The syncerebrum, also supraesophageal ganglion, consists of
cheliceral ganglia and the brain. The brain receives optic nerves and contains visual
and association centres (Foelix 2011). Despite these relatively simple and small
CNS, some spiders exhibit remarkably complex behaviours. For example, some
species are able to improve their prey capture technique with experience
(e.g. Edwards and Jackson 1994), learn to avoid dangerousprey (e.g. Higgins
2007), adjust their ghting behaviour according to their previous experiences
(e.g. Whitehouse 1997), etc.
Sensory hairs are extremely sensitive; touching a single hair causes a spider to
escape or counterattack (Foelix 2011). Given the sensitivity and importance of their
sensory organs, spiders should always be handled with care in order to prevent
damaging sensory organs and overstimulating the animals. The overstimulation of
mechanoreceptors can be avoided by keeping spiders in rooms with minimal vibra-
tional stimuli, either airborne (wind, music) or substrate borne (machines causing
vibrations). Similarly, routine tasks like cleaning the enclosures and feeding should
be done quickly and with minimal disturbance. Also, spiders should not be handled
manually, rather, we recommend using a soft brush.
5.3 The Ability to Feel Pain, Distress and Suffering
Researchers are commonly concerned about the welfare of their model animals. An
animals ability to feel pain, distress and suffering is often judged by the size and
complexity of its nervous system and/or complexity of its behaviour (Mather 2011).
Almost all animals with a nervous system can detect dangerous stimuli and will
withdraw when stimulated. In other words, they exhibit nociception, the capacity to
respond to aversive stimuli with activation of sensory and motor pathways.
5 Spider Welfare 107
Activation of the latter usually results in a reexive behavioural response. Reexive
withdrawal may be mediated by simple sensory-motor pathways without involve-
ment of higher processing centres. In this view, spiders, lacking higher nerve centres,
should only be capable of reexive behavioural responses to dangerous stimuli.
Thereby, it is more difcult to judge whether spiders experience pain, i.e. an
unpleasant sensory and emotional experience associated with actual or potential
tissue damage, or described in terms of such damage(Merskey and Bogduk 1994).
While nociception occurs with or without conscious sensation, the denition of pain
requires an emotional experience and thus consciousness. In vertebrates, the
cognitive-emotional component of pain, or simply feeling and awareness of pain,
involves higher brain structures, e.g. the limbic system, and processes. In this view,
we could conclude that the spidersnervous system precludes them to experience
any kind of mental state. However, the spidersneural architecture is not fully
understood (Jakob et al. 2011). Also, arthropods in general might possess different
neurobiological mechanisms for experiencing pain than vertebrates. In any way, the
lack of knowledge should not be an excuse to handle spiders in a way that activates
their nociceptive pathways.
Recently, additional criteria that should be fullled to accept potential pain
experience have been proposed (Elwood 2011; Sneddon et al. 2014). Sneddon
et al. (2014) stated that responses to noxious, potentially painful events should affect
neurobiology, physiology and behaviour in a different manner to innocuous stimuli,
and subsequent behaviour should be modied including avoidance learning and
protective responses. In addition, animals should show a change in motivational
state after experiencing a painful event such that future behavioural decision-making
is altered and can be measured as a change in conditioned place preference, self-
administration of analgesia, paying a cost to access analgesia or avoidance of painful
stimuli and reduced performance in concurrent events.
Following these criteria, we will examine the below features indicating the
potential for experiencing pain in spiders:
1. Nociceptors and central nervous system
2. Physiological changes to noxious stimuli
3. Protective motor reactions that might include reduced use of an affected area such
as limping, rubbing, holding or autotomy
4. Avoidance learning
5. Cognitive abilities
5.3.1 Nociceptors and Central Nervous System
There is not much known about the presence of nociceptors in spiders and how
nociceptive information is processed within their central nervous system. Neverthe-
less, spiders exhibit withdrawal or escape behaviours when exposed to noxious
stimuli. They may also exhibit behaviours that may not simply be nociceptive
108 S. Kralj-Fišer and M. Gregorič
reexes; e.g. jumping (Suter and Gruenwald 2000), shaking web (Jackson et al.
1992; Kralj-Fišer et al. 2011) and autotomy (Eisner and Camazine 1983; Punzo
1997). Their antipredator behaviour includes thanatosis (feigning deaththis behav-
iour is characterized by curling legs and freezing, resulting in a body posture very
similar to that of a dead spider) (Bilde et al. 2006; Kralj-Fišer and Schneider 2012)
and bailing out, in which the spider drops from the web and hangs motionless from
a dragline with huddled legs (Uetz et al. 2002).
5.3.2 Physiological Changes to Noxious Stimuli
Spiders detect predators by airborne vibrations stimulating their trichobothria
(Foelix 2011). The increased sensitivity of trichobothria to air movements relates
to increased octopamine (OA) levels (Widmer 2005). Octopamine in arthropods is
considered analogous to the vertebrate norepinephrine, indicating its role in the
stress system (Roeder 1999). Jones et al. (2011) experimentally elevated levels of
OA and serotonin (5-HT) in the orb web spider, Larinioides cornutus, and observed
that increased OA levels relate to decreased durations of thanatosis, while elevated
5-HT had the opposite effect (Jones et al. 2011). The elevated 5-HT likely makes the
spiders more fearful and less aggressive, whereas elevated OA likely relates to
increased arousal (Jones et al. 2011). The reductions of 5-HT and OA levels after
agonistic encounters have been observed in the brain of male bird spiders, with
subordinate males exhibiting lower levels than dominant ones (Punzo and Punzo
2001). These ndings suggest that the activation of the stress system in response to
aversive stimuli may be comparable to the one in vertebrates.
5.3.3 Protective Motor Reactions
Spiders regularly autotomize their legs when in dangerous situation, e.g. grasped by
a predator or a conspecic during ght, in order to escape more easily (Punzo 1997;
Foelix 2011). Furthermore, they self-amputate injured appendages (Kralj-Fišer et al.
2011; Kralj-Fišer and Kuntner 2012; Kuntner et al. 2014), and they lickor rub
their wounds. Missing appendages may negatively affect development, web build-
ing, foraging success, competitive abilities and mating success in some species,
whereas in several species it has no apparent costs (reviewed in Fleming et al. 2007).
Eisner and Camazine (1983) conducted an experiment that suggests a concor-
dance between pain effects in humans and autotomy in spiders. They observed
Argiope spiders that were stung in the leg by bees and wasps to undergo leg
autotomy. They experimentally penetrated the leg-joint with a sterile pin and
injected spiders with several venom components known to elicit pain in humans.
Spiders employed autotomy when injected with histamine, serotonin, phospholipase
and melittin, all of which induce pain in humans. Acetylcholine and bradykinin,
5 Spider Welfare 109
which also induce pain in humans, did not cause the autotomy in spiders. However,
injection of hyaluridase, adrenaline and dopamine, which do not induce pain in
humans, also failed to be effective in causing autotomy in Argiope.
5.3.4 Avoidance Learning
Avoidance learning is the process by which an individual learns to avoid unpleasant
situations on the basis of prior experience. There is abundant evidence for avoidance
learning in spiders. For example, the wolf spider Schizocosa avida exhibits associa-
tive learning in response to previous experience with a predator (Punzo 1997).
Individuals of the same species that have survived a scorpion attack by leg autotomy
learn to avoid scorpion-scented substrates (Punzo 1997).
Several spiders are able to develop aversion to toxic and/or unpalatable prey
(e.g. Edwards and Jackson 1994; Toft and Wise 1999; Skow and Jakob 2006;
Hénaut et al. 2014). Furthermore, jumping spiders exhibit avoidance of visual
stimuli associated with heat (Nakamura and Yamashita 2000), electric shock
(Bednarski et al. 2012; Peckmezian and Taylor 2015) or vibration (Long et al.
2015). For example, jumping spiders of the species Hasarius adansoni were trained
to associate heat with coloured papers. These spiders learned to avoid colours which
were associated with high temperature, suggesting that they are not just able to learn
to avoid heat but also to associate it with colour (Nakamura and Yamashita 2000).
Thus, spiders are likely able to learn and take the appropriate action to avoid or
reduce potential damage on the basis of prior experience with noxious stimuli; such a
response is not the xed, reexive action of nociceptive avoidance.
5.3.5 Cognitive Abilities
There is ample of evidence indicating spidersability to learn. Several species are
able to (adaptively) modify their behaviour in the contexts of foraging (e.g. Wilcox
and Jackson 1993) and web building (e.g. Heiling and Herberstein 1999; Venner
et al. 2000), intraspecic interactions (e.g. Taylor and Jackson 2003; Kasumovic
et al. 2009), spatial learning and navigation (Tarsitano and Jackson 1997; Jakob et al.
2007). Some spiders even exhibit reversal learning (Liedtke and Schneider 2014).
For a more exhausted literature on evidence for behavioural plasticity, learning,
memory and other cognitive abilities in spiders, see reviews by Jackson and Cross
(2011), Jakob et al. (2011), Nelson and Jackson (2011) and Japyassú and
Laland (2017).
110 S. Kralj-Fišer and M. Gregorič
5.4 Keeping Spiders in Captivity
To secure the well-being of animals in captivity, we have to satisfy their general
needs, e.g. ready access to fresh water; a balanced diet; appropriate housing;
prevention from pain, injury or disease; and enabling an environment to express
normal behaviours and ensure conditions and treatments causing no/little fear and
stress. Ethical guidelines for research in vertebrates follow the three Rs(3Rs)
principle, i.e. the replacement, reduction and renement criteria (Russell and Burch
1959). While the latter two should be applied to spiders, the rst likely does not.
Replacement generally refers to replacing animals with non-sentient material
(Russell and Burch 1959), e.g. plants, microorganisms, animals with limited nervous
and sensory systems, tissue cultures and computer models (Tannenbaum and Ben-
nett 2015). Similarly, loweranimals like arthropods are considered a replacement
for higherones, e.g. mammals, with the justication of evolutionary conservation
of physiological processes allowing for application across animal groups (Horvath
et al. 2013). Replacing arthropods for vertebrates might be argued for in some
contexts, e.g. when experimental procedures involve trauma, and keeping a large
number of experimental animals. However, arthropods and thus spiders can hardly
be replaced by other animals, especially considering the gaps in our knowledge in
these loweranimal groups. These same knowledge gaps currently render replacing
spiders with other invertebrates, tissue cultures and computer models impossible.
The reduction and renement principles apply to animal experiments in general and
thus have to be taken into account in spider research. Reduction refers to using the
minimal number of animals required to perform a study, where careful experimental
and statistical planning is crucial. Renement generally refers to nding experimen-
tal designs that maximize the scientic output while minimizing negative effects on
animals, e.g. by planning for potential experimental problems, choosing the least
invasive techniques and ensuring proper housing (Animal Behaviour 2018).
Until recently, the welfare of spiders and most other invertebrates in captivity has
been neglected. Several invertebrate species have long been used as model organ-
isms in research, to full the replacementcriterion in animal welfare guidelines for
vertebrates (Carere et al. 2011). Do spiders and other invertebrates indeed suffer less
and are they more suitable for life in captivity than vertebrates? Can we further
ignore the fact that spiders full several criteria that indicate their potential for
experiencing pain? Instead, researchers should use the existing knowledge to estab-
lish standards for securing their welfare.
The responsibilities of researchers to take care for study animals do not only
include the experimental procedures themselves but extend to providing suitable
conditions at which spiders are bred or kept when not being studied. To maximize
welfare, the housing of spiders should incorporate as many of the important natural
living conditions as possible. While the general seasonal parameters, e.g. the
day/night regime, temperature and relative humidity, can be mimicked by knowing
a spiders habitat and diurnal cycle, other maintenance parameters are important.
Researchers should consider the importance of the size of enclosure, providing
5 Spider Welfare 111
biologically relevant enrichment and social interactions among individuals, as well
as proper nutrition and euthanasia, all of which are discussed in the following
5.4.1 Husbandry
Spiders in general can be divided into two basic life style groups, the cursorial and
web-building spiders, and within both of these several subcategories can be identi-
ed. For example, some cursorial species are completely ground dwelling, while
others are arboreal, but most inhabit diverse habitats that cannot be classied into
such extremes. Thus, maximizing the enclosuresoor space and climbing space or
providing other enrichments is crucial. Similarly, some web-building spiders employ
two-dimensional orb webs, while others employ three-dimensional webs. Thus, orb
weavers can be efciently kept in frames, usually piled like books on shelves,
maximizing laboratory space and allowing the spiders to build webs (Fig. 5.1). On
the other hand, three-dimensional webs demand cubic-shaped enclosures (Fig. 5.2),
sometimes with supporting structures allowing web construction (Zschokke and
Herberstein 2005).
While it is straightforward that larger spider species need to be housed in larger
enclosures, it is sometimes difcult to identify biologically meaningful enrichment
features for certain species, especially if their natural history is little known or they
have not been previously kept in the laboratory. Web building spiders almost
exclusively live on their webs. They either sit in the web itself or construct retreats
in or at the side of the web. Thus, it is relatively easy to recognize such biologically
meaningful enrichment features while collecting them in the eld (e.g. providing
shelters or materials for shelters). On the other hand, cursorial spiders are usually
housed in simple enclosures, out of practicality often without enrichment features
(e.g. easier observation, cleanliness (Jackson 1974). However, it is almost unknown
how housing conditions affect cursorial spiders. There is evidence that environmen-
tal stimuli can inuence behavioural syndromes, and thus laboratory-bred individ-
uals differ from eld-caught ones (Sweeney et al. 2013). This might be especially
Fig. 5.1 Frame-shaped enclosures allow the construction of two-dimensional orb webs (a), can be
made from Perspex (b), plastic mesh (c) or any other suitable material and are suitable for
maximizing laboratory space (b, c)
112 S. Kralj-Fišer and M. Gregorič
important in taxa with well-developed cognitive abilities, e.g. jumping spiders,
although little is known about cognitive abilities of most other spider groups. In
fact, laboratory raising jumping spiders of the species Marpissa muscosa in envi-
ronmentally deprived, socially enriched or physically enriched enclosures consis-
tently affects their personality traits (Liedtke et al. 2015; see Carere and Maestripieri
2013). Furthermore, recent research demonstrates neuroplasticity in jumping spiders
by showing that M. muscosa spiders growing up solitary and in physically deprived
enclosures have smaller volumes of higher order integrating brain centres compared
to spiders growing up with siblings or in physically enriched enclosures (Steinhoff
et al. 2018). These brain centres, composed of mushroom bodies and the arcuate
body, receive visual and maybe also locomotory information and process it
(Steinhoff et al. 2017). Both in vertebrates and arthropods, the variation in cognitive
ability, and thus behaviour, seems to be directly inuenced by brain size (Amador-
Vargas et al. 2015; Benson-Amram et al. 2016; Corral-López et al. 2017; Feinerman
and Traniello 2016). This highlights the need for further studies of how laboratory
conditions affect the spider nervous system. Moreover, while spiders are generally
considered solitary and intolerant of conspecics, several species do live in aggre-
gations, and some are even (sub)social (Foelix 2011).
Proper housing, be it through providing biologically meaningful enclosure
enrichments or social interactions, can thus not only assure the animalswell-
being but also minimizes potential factors affecting their behaviour in experiments.
Furthermore, spiders are often kept permanently as laboratory model animals.
Maintaining a healthy laboratory population can reduce the amount of needed
wild-caught animals and allows the researchers to comply with the reduction
and renementprinciples of the 3Rs guiding principles for appropriate animal
care. Namely, it is critical to choose correct experimental and statistical procedures,
as well as planning and conducting experiments in a way to maximize the scientic
benet. Through keeping a predictable laboratory population of model taxa, one can
Fig. 5.2 Cubic-shaped enclosures (b) with supporting structures (a) that allow the construction of
three-dimensional cobwebs
5 Spider Welfare 113
overall reduce the number of spiders in experiments to the lowest number necessary
to achieve experimental goals while ensuring the highest quality standards for the
kept animals.
5.4.2 Nutrition
Nutrition importantly inuences nearly all aspects of an individuals life history.
Starvation and low food quality (i.e. nutrient imbalance and/or deciency) are
independent stressful conditions, and spiders can suffer from one or both (Toft
2013). The amount of food affects the rate of growing, adult size, lifespan and
fecundity (Yip and Lubin 2016). Generally, smaller amounts of food increase
developmental time and sometimes the number of instars, often leading to smaller
adult body size, which in females is positively correlated with the number and/or
biomass of produced eggs (Jakob and Dingle 1990; Vollrath 1987). Both prolonged
developmental time and smaller and fewer eggs can mean heavy tness penalties
(Higgins 1995; Higgins and Goodnight 2011). Unless the experimental procedure
demands otherwise, laboratory-kept spiders are generally fed ad libitum because
assuring enough prey is not problematic. When providing laboratory-bred insect
food, its diversity is usually lower than most natural conditions. Small instar spiders
are typically fed with fruit ies or springtails, and larger spiders with house ies,
mealworms and crickets. However, although a small food diversity could imply poor
nutrition, it is not necessarily so. Inappropriate prey taxa can have an imbalanced
nutrient composition or might even contain toxins and deterrents in too high
amounts. Furthermore, an imbalanced nutrient composition and toxicity are not
intrinsic to food items but properties of the consumers physiology, i.e. the specic
spider species (Toft 2013).
Food quality is best dened with its potential contribution to the tness of the
consumer. Because a certain prey taxon can be appropriate for some, but not other
spider species, food quality cannot easily be determined using a chemical analysis
but is best determined in tness performance experiments. In these, the effect of
single-prey diets is compared to high-quality control food and starvation (Toft
2013). Tests of multiple prey taxa have shown a continuum of prey qualities,
classied into high-quality,intermediate-quality,low-quality,poor-quality
and toxicprey taxa. Only prey classied as high quality allows spiders on a
monotypic diet a full life cycle with low mortality and successful reproduction
(Toft 2013). Some prey taxa, e.g. aphids, seem to generally be of very low food
quality to spiders, while others, e.g. Diptera and Collembola, seem to cover the
whole spectrum of the needed nutritional composition and may be classied as high
quality for most spider species (Schmidt et al. 2012; Toft and Wise 1999). A logical
advice for proper spider nutrition is thus introducing known high-quality prey taxa
even when keeping spiders that have not been nutritionally investigated before.
Additional food enrichment can be achieved by keeping spiders on a multi-prey
diet or by enriching the food of prey. For example, growth media of prey like fruit
114 S. Kralj-Fišer and M. Gregorič
ies can be enriched with multiple or single nutrients, e.g. protein, lipids and
vitamins. Similarly, adding dog food to the growth medium of prey like springtails,
fruit ies, house ies and crickets proved successful (Toft 2013).
In recent years, the effects of nutrient composition on physiology and behaviour
of spiders are getting better documented. For example, protein addition increases
growth and the building of stabilimenta in the orb weaver Argiope keyserlingi
(Blamires et al. 2009), while it decreases glue stickiness in the orb weaver Nephila
clavipes and cob web Latrodectus hesperus (Blamires et al. 2014). Also, the protein
content in food is positively correlated with growth rate in Pardosa prativaga
(Jensen et al. 2011), but not in Stegodyphus lineatus, where lipids promote growth,
but protein addition enhances juvenile survival (Salomon et al. 2008; Salomon et al.
2011). Unfortunately, we currently do not fully understand how nutrient demands
differ among spider species and how ontogenetic stage and seasonality affect them
intraspecically. As mentioned above, starvation and nutrient imbalance represent
independent stress factors (Toft 2013). In the laboratory, one can easily prevent
starvation. However, well-fed spiders, i.e. such with a high body condition index
(body mass regressed to body size), are not necessarily also receiving a balanced diet
(Lomborg and Toft 2009; Wilder and Rypstra 2008), and there is currently no quick
and easy way to assess possible nutrient imbalance. Thus, to ensure the functional
denition of high-quality nutrition, laboratory-kept spiders need to be offered food
that allows a full life cycle with low mortality and successful reproduction.
5.4.3 Disease Monitoring and Disposal
Like all arthropods and most invertebrates, spiders have an open circulatory system,
where the haemolymph ows via a closed arterial system and an open venous system
(Foelix 2011). Physical injuries are followed by haemolymph loss and expose
spiders to microbial infections. Thus, the spiders immune system is composed of
haemolymph coagulation and pathogen-defence that is localized in haemocytes. The
immune system rapidly reacts to invasion, releasing several compounds into the
haemolymph in a matter of minutes to hours, and comprises a clotting cascade to
stop haemolymph loss, phagocytosis, the regulation of pathogen-destroying melanin
production and the production of antimicrobial peptides (Kuhn-Nentwig and
Nentwig 2013). To the best of our knowledge, the effects of diverse laboratory
conditions on spider immune system appear unknown. Similarly, disease treatment
is not developed, likely in large part because identication of a disease is mostly
possible only in its latest stages of conspicuous symptoms or when spider behaviour
changes drastically. Researchers thus mostly have to do their best to prevent disease.
When choosing enclosure enrichment, it is advisable to clean, dry out or otherwise
disinfect any material from nature. Prey should consist of laboratory-bred insects to
prevent introducing pathogens or parasites. The enclosures should be kept as clean
as possible, and especially when high humidity is necessary, air circulation needs to
be ensured to minimize mould. However, the frequency of enclosure cleaning should
5 Spider Welfare 115
represent a compromise between the level of required cleanliness and the amount of
disturbance imposed to the spider.
Another important consideration is what happens to spiders after they die or after
the end of experiments. Spiders that clearly died of disease should be disposed
according to local waste handling procedures. On the other hand, it is likely safe to
dispose spiders that died naturally as usual biological waste, as research on spiders
usually does not include hazards occurring in other elds, e.g. dangerous chemicals
(sterilants, disinfectants) and microorganisms, allergens and radiologic agents. If
spiders are released after the experiments, they should be released where caught, and
in the correct part of season based on their developmental stage. Released spiders
should also not be in a state that will harm the natural population (e.g. because of
disease or genetic modication).
5.4.4 Anaesthesia and Euthanasia
Due to a lack of research on invertebrate anaesthesia, analgesia and euthanasia, these
elds are getting increasingly debated (Bennie et al. 2012; Cooper 2011) and are
tightly linked to the issue of how animals perceive stress and pain (see Spiders
ability to feel pain, distress and suffering). Anaesthesia in spiders is usually
employed to immobilize the animals, in order to facilitate tagging (e.g. for the
need of individual recognition in experiments), examination (e.g. to determine the
species, check for genital details) and to perform different procedures (e.g. obtain
silk or venom). In terrestrial invertebrates, isourane (510%), sevourane, halo-
thane (510%) or carbon dioxide (CO
,1020%) are the suggested agents for
anaesthesia (Cooper 2011). In our experience, the most common agent in spider
laboratories is CO
. While the suggested concentration of CO
is 1020%, spider
laboratories use a wide variety of concentration, always with fast recovery, and
without mortality and visible long-term consequences. However, if anaesthetized
spiders are used for potentially painful procedures, CO
is not advised as it is
unknown to what extent, if, any at all, it induces analgesia. In such cases, using
isourane, halothane or sevourane is advised, with isourane being the preferred in
terrestrial arthropods in general (Cooper 2011) and also successfully employed in
spiders (Pizzi 2006). Hypothermia is a traditional anaesthesia method in invertebrate
studies but generally of limited use (Cooper 2011) and not advised in spider
research. While it might be of use for some noninvasive procedures, it should not
be used for invasive ones, and we generally advise against it in arachnids as many
seem to not tolerate chilling well and can even die (Pizzi 2006). To avoid compli-
cations during anaesthesia, one should avoid employing it in individuals of visibly
poor body conditions or otherwise unhealthy.
Some research elds and methods cannot avoid sacricing a certain number of
individuals. If spiders get euthanized, researchers have to state why and describe the
method. A gooddeath is an inseparable part of a goodlife for all captive
animals. A variety of methods of invertebrate euthanasia are described in the
116 S. Kralj-Fišer and M. Gregorič
literature, ranging from decapitation and injection of chemicals to freezing and
immersion in ethanol, but most have not been properly studied (Cooper 2011;
Lewbart 2011). Suitable methods of euthanasia need to be effective and simple to
perform and cause the least distress to the animal, and they have to be compatible
with given research method if performed for that reason (Bennie et al. 2012). For
example, Bennie et al. (2012) suggest terrestrial arthropod euthanasia through
targeted hyperkalosis, i.e. injection of potassium chloride to depolarize the tho-
racic ganglia, causing rapid death. While this method has been successfully tested on
a variety of terrestrial arthropods, including a scorpion, it will likely not be widely
used in spiders as many spider species are too small in size, many research elds
operate with too many animals for individual injections, or the eld conditions
would make such a method inconvenient. For spiders, Pizzi (2006) recommends
immersion in 70% ethanol and warns against freezing, as the latter can compromise
subsequent histological examination. In fact, the most common euthanasia method
in spiders is immersion in ethanol as it is compatible with most research elds. In
some elds, especially the ones relying on molecular data, freezing is necessary, be it
without a medium or submerged in ethanol or buffer. Other elds (e.g. systematics
and taxonomy, behavioural sciences) sometimes necessitate the euthanasia of a
number of individuals to store as vouchers, without the need for subsequent exper-
iments. In such cases, one should choose the more humane method, even if
compromising tissues. For example, when euthanizing spiders to store in ethanol,
it might be more humane to rst anaesthetize them using CO
, low percent ethanol or
instant deep-freezing (60 Cto80 C) and subsequently transfer them into
ethanol for preservation. In fact, a recent study shows a two-step method of rst
anaesthetizing gastropods in 5% ethanol for later preservation in 7095% ethanol, to
be the most appropriate (Gilbertson and Wyatt 2016). Unfortunately, as is true for
most invertebrates in general, euthanasia methods for spiders are inadequately
researched and necessitate much more attention.
5.5 Conclusions
Spiders are often used as research models and for biodiversity displays while also
kept as pets. Due to anthropocentric views on invertebrates, spiders are historically
considered as automata, but the growing evidence shows that spiders are not purely
instinctive but exhibit behavioural plasticity including learning. This evidence must
not be further ignored, and setting the standards for securing spiderswelfare in
captivity is needed, in order to comprehend (1) if/when spider feel pain and distress
and (2) what we can do to avoid or minimize it.
1. Humans commonly regard spiders as animals without the capacity to experience
pain, and their responses are considered as purely nociceptive reexes. This
reasoning is based on the fact that spiders lack the brain regions implicated in
pain processing found in higher vertebrates. They might, however, possess
5 Spider Welfare 117
neurobiological mechanisms for experiencing pain different than vertebrates.
Recent denitions of a possible pain experience include criteria such as appro-
priate nociceptors and a central nervous system, physiological changes to noxious
stimuli, protective motor reactions that might include reduced use of an affected
area (e.g. limping, rubbing, holding, autotomy), avoidance learning and cognitive
abilities (Elwood 2011; Sneddon et al. 2014). We present here what criteria for
potential experience of pain have been found in spiders.
In spiders, little is known about the presence of nociceptors and how nocicep-
tive information is processed within their central nervous system. Besides
exhibiting withdrawal or escape behaviours when exposed to noxious stimuli,
spider avoidance includes behaviours that may not simply be nociceptive
reexes, e.g. jumping, shaking web, autotomy and thanatosis. Spiders detect
predators or other potential aversive stimuli by airborne vibrations stimulating
their trichobothria. Increased trichobothria stimulation relates to increased levels
of octopamine, which is considered analogous to the vertebrate norepinephrine,
indicating its role in the stress system in spiders. Spiders also exhibit protective
motor reactions. They commonly autotomize their legs when in dangerous
situation, e.g. grasped by a predator, in order to escape. Furthermore, they self-
amputate injured appendages, and they lickor rub their wounds. An interesting
experiment by Eisner and Camazine (1983) even suggests a concordance between
pain effects in humans and autotomy in spiders. There is also abundant evidence
for avoidance learning in spiders. Studies show that spiders are able to learn and
take the appropriate action to avoid or reduce potential damage on the basis of
prior experience with noxious stimuli. Such a response is not the xed, reexive
action of nociceptive avoidance. Furthermore, there is ample evidence of the
ability of spiders to learn. Several species are able to modify their behaviour in
contexts of foraging and web building, intraspecic interactions, spatial learning
and navigation.
2. To secure animal well-being in captivity, we have to satisfy their general needs.
Thus, spiders need access to fresh water and a balanced nutrition and appropriate
housing with biologically meaningful enrichments, and keeping should prevent
pain, injury and disease, all of which enable an environment to express normal
behaviours and ensure that conditions and treatments cause no/little fear and
stress. In spider research, we need to follow the general ethical guidelines for
animal care, i.e. the 3Rs principle. However, researchers using spiders as
experimental subject need to follow the general reduction and renement guide-
lines, while the replacement guideline (i.e. replacing animals with tissue cultures
and computer models) is currently likely not applicable.
Additionally, some research elds cannot avoid anaesthetizing and/or sacricing
spiders. In spiders, using CO
for anaesthesia generally seems to enable fast recovery
and no visible long-term consequences, while for potentially painful procedures,
isourane, halothane or sevourane is preferred. The most common euthanasia
method in spiders is immersion in ethanol as it is compatible with most research
elds, but when the research protocol permits it, one should choose a more humane
118 S. Kralj-Fišer and M. Gregorič
method. For example, when euthanizing spiders to store in ethanol, it might be more
humane to rst anaesthetize them using CO
, low percent ethanol or instant deep-
freezing and subsequently transfer them into ethanol for preservation.
While there are well-dened ethical guidelines for using vertebrates in research,
welfare in invertebrates is minimally regulated and generally neglected by
researchers. To address the numerous knowledge gaps in our understanding of
welfare in invertebrates, we rst need to set clearly dened criteria of how to assess
experiences of pain and suffering in a given invertebrate group. Such denitions will
allow us to set clearly dened hypotheses that can be experimentally tested. Despite
this need for research, by following the above guidelines, we can avoid at least the
known sources of distress in spiders.
Amador-Vargas S, Gronenberg W, Wcislo WT, Mueller U (2015) Specialization and group size:
brain and behavioral correlates of colony size in ants lacking morphological astes. Proc R Soc B
Biol Sci 282:20142502
Animal Behaviour (2018) Guidelines for the treatment of animals in behavioural research and
teaching. Anim Behav 135:IX
Barth FG (2013) A spiders world: senses and behavior. Springer, Berlin
Bednarski JV, Taylor P, Jakob EM (2012) Optical cues used in predation by jumping spiders,
Phidippus audax (Araneae, Salticidae). Anim Behav 84:12211227
Bennie N, Loaring C, Bennie M, Trim S (2012) An effective method for terrestrial arthropod
euthanasia. Anim Technol Welf 215:42374241
Benson-Amram S, Dantzer B, Stricker G, Swanson EM, Holekamp KE (2016) Brain size predicts
problem-solving ability in mammalian carnivores. Proc Natl Acad Sci 113:25322537
Bilde T, Tuni C, Elsayed R, Pekár S, Toft S (2006) Death feigning in the face of sexual cannibalism.
Biol Lett 2:2325
Blamires SJ, Hochuli DF, Thompson MB (2009) Prey protein inuences growth and decoration
building in the orb web spider Argiope keyserlingi. Ecol Entomol 34:545550
Blamires SJ, Sahni V, Dhinojwala A, Blackledge TA, Tso IM (2014) Nutrient deprivation induces
property variations in spider gluey silk. PLoS One 9:e88487
Blest AD, Hardie RC, McIntyre P, Williams DS (1981) The spectral sensitivities of identied
receptors and the function of retinal tiering in the principal eyes of a jumping spider. J Comp
Physiol A 145:227239
Carere C, Maestripieri D (2013) Animal personalities: behavior, physiology, and evolution. Uni-
versity of Chicago Press, Chicago
Carere C, Wood JB, Mather J (2011) Species differences in captivity: where are the invertebrates?
Trends Ecol Evol 26:211
Coddington JA, Levi HW (1991) Systematics and evolution of spiders (Araneae). Annu Rev Ecol
Syst 22:565592
Cooper JE (2011) Anesthesia, analgesia, and euthanasia of invertebrates. ILAR J 52:196204
Corral-López A, Bloch NI, Kotrschal A, Van Der Bijl W, Buechel SD, Mank JE, Kolm N (2017)
Female brain size affects the assessment of male attractiveness during mate choice. Sci Adv 3:
Edwards GB, Jackson RR (1994) The role of experience in the development of predatory behaviour
in Phidippus regius, a jumping spider (Araneae, Salticidae) from Florida. N Z J Zool
5 Spider Welfare 119
Eisner T, Camazine S (1983) Spider leg autotomy induced by prey venom injection: an adaptive
response to pain? Proc Natl Acad Sci 80:33823385
Elwood RW (2011) Pain and suffering in invertebrates? ILAR J 52:175184
Feinerman O, Traniello JFA (2016) Social complexity, diet, and brain evolution: modeling the
effects of colony size, worker size, brain size, and foraging behavior on colony tness in ants.
Behav Ecol Sociobiol 70:10631074
Fleming PA, Muller D, Bateman PW (2007) Leave it all behind: a taxonomic perspective of
autotomy in invertebrates. Biol Rev 82:481510
Foelix RF (2011) Biology of spiders, 3rd edn. Oxford University Press, New York
Gilbertson CR, Wyatt JD (2016) Evaluation of euthanasia techniques for an invertebrate species,
land Snails (Succinea putris). J Am Assoc Lab Anim Sci 55:577581
Heiling AM, Herberstein ME (1999) The role of experience in web-building spiders (Araneidae).
Anim Cogn 2:171177
Hénaut Y, Machkour-MRabet S, Lachaud JP (2014) The role of learning in risk-avoidance
strategies during spider-ant interactions. Anim Cogn 17:185195
Herberstein ME (2011) Spider behaviour: exibility and versatility. Cambridge University Press,
Higgins L (1995) Direct evidence for trade-offs between foraging and growth in a juvenile spider.
J Arachnol 23:3743
Higgins L (2007) Juvenile Nephila (Araneae, Nephilidae) use various attack strategies for novel
prey. J Arachnol 35:530534
Higgins L, Goodnight C (2011) Developmental response to low diets by giant Nephila clavipes
females (Araneae: Nephilidae). J Arachnol 1:399408
Horvath K, Angeletti D, Nascetti G, Carere C (2013) Invertebrate welfare: an overlooked issue. Ann
Ist Super Sanita 49:917
Jackson RR (1974) Rearing methods for spiders. J Arachnol 2:5356
Jackson RR, Cross FR (2011) Spider cognition. Adv Insect Physiol 41:115174
Jackson RR, Rowe RJ, Campbell GE (1992) Anti-predator defences of Psilochorus sphaeroides
and Smeringopus pallidus (Araneae, Pholcidae), tropical web-building spiders. J Zool
Jakob EM, Dingle H (1990) Food level and life history characteristics in a pholcid spider
(Holocnemus pluchei). Psyche 97:95110
Jakob EM, Skow CD, Haberman MP, Plourde A (2007) Jumping spiders associate food with color
cues in a T-Maze. J Arachnol 35:487492
Jakob E, Skow C, Long S (2011) Plasticity, learning and cognition. In: Herberstein ME (ed) Spider
behaviour: exibility and versatility. Cambridge University Press, Cambridge, pp 307347
Japyassú HF, Laland KN (2017) Extended spider cognition. Anim Cogn 20:375395
Jensen K, Mayntz D, Toft S, Raubenheimer D, Simpson SJ (2011) Nutrient regulation in a predator,
the wolf spider Pardosa prativaga. Anim Behav 81:993999
Jones TC, Akoury TS, Hauser CK, Neblett MF II, Linville BJ, Edge AA, Weber NO (2011)
Octopamine and serotonin have opposite effects on antipredator behavior in the orb-weaving
spider, Larinioides cornutus. J Comp Physiol A 197:819825
Kasumovic MM, Elias DO, Punzalan D, Mason AC, Andrade MCB (2009) Experience affects the
outcome of agonistic contests without affecting the selective advantage of size. Anim Behav
Kralj-Fišer S, Kuntner M (2012) Eunuchs as better ghters? Naturwissenschaften 99:95101
Kralj-Fišer S, Schneider JM (2012) Individual behavioural consistency and plasticity in an urban
spider. Anim Behav 84:197204
Kralj-Fišer S, GregoričM, Zhang S, Li D, Kuntner M (2011) Eunuchs are better ghters. Anim
Behav 81:933939
Kuhn-Nentwig L, Nentwig W (2013) The immune system of spiders. In: Nentwig (ed) Spider
ecophysiology. Springer, Berlin, pp 8191
120 S. Kralj-Fišer and M. Gregorič
Kuntner M, Pristovšek U, Cheng RC, Li D, Zhang S, Tso IM, Liao CP, Miller JA, Kralj-Fišer S
(2014) Eunuch supremacy: evolution of post-mating spider emasculation. Behav Ecol Sociobiol
Lewbart GA (2011) Invertebrate medicine, 2nd edn. Blackwell Publishing, Ames
Liedtke J, Schneider JM (2014) Association and reversal learning abilities in a jumping spider.
Behav Processes 103:192198
Liedtke J, Redekop D, Schneider JM, Schuett W (2015) Early environmental conditions shape
personality types in a jumping spider. Front Ecol Evol 3:134
Lomborg JP, Toft S (2009) Nutritional enrichment increases courtship intensity and improves
mating success in male spiders. Behav Ecol 20:700708
Long SM, Leonard A, Carey A, Jakob EM (2015) Vibration as an effective stimulus for aversive
conditioning in jumping spiders. J Arachnol 43:111114
Mather J (2011) Philosophical background of attitudes toward and treatment of invertebrates. ILAR
J 52:205212
Merskey H, Bogduk N (1994) Classication of chronic pain: description of chronic pain syndromes
and denitions of pain terms. IASP Press, Seattle
Nakamura T, Yamashita S (2000) Learning and discrimination of colored papers in jumping spiders
(Araneae, Salticidae). J Comp Physiol 186:897901
Nelson XJ, Jackson RR (2011) Flexibility in the foraging strategies of spiders. In: Herberstein ME
(ed) Spider behaviour: exibility and versatility. Cambridge University Press, Cambridge, pp
Nyffeler M, Birkhofer K (2017) An estimated 400800 million tons of prey are annually killed by
the global spider community. Sci Nat 104:30
Peckmezian T, Taylor PW (2015) Electric shock for aversion training of jumping spiders: towards
an arachnid model of avoidance learning. Behav Processes 113:99104
Pizzi R (2006) Spiders. In: Lewbart GA (ed) Invertebrate medicine. Blackwell, Ames, pp 143168
Punzo F (1997) Leg autotomy and avoidance behavior in response to a predator in the wolf spider,
Schizocosa avida (Araneae, Lycosidae). J Arachnol 25:202205
Punzo F, Punzo T (2001) Monoamines in the brain of tarantulas (Aphonopelma hentzi) (Araneae,
Theraphosidae): differences associated with male agonistic interactions. J Arachnol 29:388395
Roeder T (1999) Octopamine in invertebrates. Prog Neurobiol 59:533561
Russell WMS, Burch RL (1959) The principles of humane experimental technique. Methuen,
Salomon M, Mayntz D, Lubin Y (2008) Colony nutrition skews reproduction in a social spider.
Behav Ecol 19:605611
Salomon M, Mayntz D, Toft S, Lubin Y (2011) Maternal nutrition affects offspring performance via
maternal care in a subsocial spider. Behav Ecol Sociobiol 65:11911202
Schmidt JM, Sebastian P, Wilder SM, Rypstra AL (2012) The nutritional content of prey affects the
foraging of a generalist arthropod predator. PLoS One 7:e49223
Skow CD, Jakob EM (2006) Jumping spiders attend to context during learned avoidance of
aposematic prey. Behav Ecol 17:3440
Sneddon LU, Elwood RW, Adamo SA, Leach MC (2014) Dening and assessing animal pain.
Anim Behav 97:201212
Steinhoff PO, Sombke A, Liedtke J, Schneider JM, Harzsch S, Uhl G (2017) The synganglion of the
jumping spider Marpissa muscosa (Arachnida: Salticidae): insights from histology, immuno-
histochemistry and microCT analysis. Arthropod Struct Dev 46:156170
Steinhoff PO, Liedtke J, Sombke A, Schneider JM, Uhl G (2018) Early environmental conditions
affect the volume of higher-order brain centers in a jumping spider. J Zool 304:182192
Suter RB, Gruenwald J (2000) Predator avoidance on the water surface? Kinematics and efcacy of
vertical jumping by Dolomedes (Araneae, Pisauridae). J Arachnol 28:201210
Sweeney K, Gadd RDH, Hess ZL, Mcdermott DR, Macdonald L, Cotter P, Armagost F, Chen JZ,
Berning AW, Dirienzo N, Pruitt JN (2013) Assessing the effects of rearing environment, natural
5 Spider Welfare 121
selection, and developmental stage on the emergence of a behavioral syndrome. Ethology
Tannenbaum J, Bennett TB (2015) Russell and Burchs 3Rs then and now: the need for clarity in
denition and purpose. J Am Assoc Lab Anim Sci 54:120132
Tarsitano MS, Jackson RR (1997) Araneophagic jumping spiders discriminate between detour
routes that do and do not lead to prey. Anim Behav 53:257266
Taylor PW, Jackson RR (2003) Interacting effects of size and prior injury in jumping spider
conicts. Anim Behav 65:787794
Toft S (2013) Nutritional aspects of spider feeding. In: Nentwig W (ed) Spider ecophysiology.
Springer, Berlin, pp 373384
Toft S, Wise DH (1999) Growth, development, and survival of a generalist predator fed single- and
mixed-species diets of different quality. Oecologia 119:198207
Uetz GW, Roberts JA (2002) Multisensory cues and multimodal communication in spiders: insights
from video/audio playback studies. Brain Behav Evol 59:222230
Uetz GW, Boyle J, Hieber CS, Wilcox RS (2002) Antipredator benets of group living in colonial
web-building spiders: the early warningeffect. Anim Behav 63:445452
Venner S, Pasquet A, Leborgne R (2000) Web-building behaviour in the orb-weaving spider
Zygiella x-notata:inuence of experience. Anim Behav 59:603611
Vollrath F (1987) Growth, foraging and reproductive success. In: Nentwig W (ed) Ecophysiology
of spiders. Springer, Berlin, pp 357370
Whitehouse MEA (1997) Experience inuences male-male contests in the spider Argyrodes
antipodiana (Theridiidae: Araneae). Anim Behav 53:913923
Widmer A (2005) Spider peripheral mechanosensory neurons are directly innervated and modu-
lated by octopaminergic efferents. J Neurosci 25:15881598
Wilcox RS, Jackson RR (1993) Spider exibly chooses aggressive mimicry signals for different
prey by trial and error. Behaviour 127:2136
Wilder SM, Rypstra AL (2008) Diet quality affects mating behaviour and egg production in a wolf
spider. Anim Behav 76:439445
World Spider Catalog (2018) World spider catalog. Version 19.5. Natural History Museum Bern. Accessed 14 Nov 2018
Yip EC, Lubin Y (2016) Effects of diet restriction on life history in a sexually cannibalistic spider.
Biol J Linn Soc 118:410420
Zschokke S, Herberstein ME (2005) Laboratory methods for maintaining and studying
web-building spiders. J Arachnol 33:205213
122 S. Kralj-Fišer and M. Gregorič
Full-text available
Designs perfected through evolution have informed bioinspired animal‐like robots that mimic the locomotion of cheetahs and the compliance of jellyfish; biohybrid robots go a step further by incorporating living materials directly into engineered systems. Bioinspiration and biohybridization have led to new, exciting research, but humans have relied on biotic materials—non‐living materials derived from living organisms—since their early ancestors wore animal hides as clothing and used bones for tools. In this work, an inanimate spider is repurposed as a ready‐to‐use actuator requiring only a single facile fabrication step, initiating the area of “necrobotics” in which biotic materials are used as robotic components. The unique walking mechanism of spiders—relying on hydraulic pressure rather than antagonistic muscle pairs to extend their legs—results in a necrobotic gripper that naturally resides in its closed state and can be opened by applying pressure. The necrobotic gripper is capable of grasping objects with irregular geometries and up to 130% of its own mass. Furthermore, the gripper can serve as a handheld device and innately camouflages in outdoor environments. Necrobotics can be further extended to incorporate biotic materials derived from other creatures with similar hydraulic mechanisms for locomotion and articulation. This work introduces a new area of research where biotic materials are used directly as actuators with minimal fabrication steps required. Taking advantage of the spider's hydraulic mechanism for leg extension, a fully functional pneumatic necrobotic gripper is fabricated in a single step by inserting a needle into the body of a deceased spider.
Full-text available
As predators, the macronutrients spiders extract from their prey play important roles in their mating and reproduction. Previous studies of macronutrients on spider mating and reproduction focus on protein, the potential impact of prey lipid content on spider mating and reproduction remains largely unexplored. Here we tested the influence of prey varying in lipid content on female mating, sexual cannibalism, reproduction and offspring fitness in the wolf spider Pardosa pseudoannulata. We acquired two groups of fruit fly Drosophila melanogaster that differed significantly in lipid but not protein content by supplementing cultural media with a high or low dose of sucrose on which the fruit flies were reared (HL: high lipid; LL: low lipid). Subadult (i.e., one molt before adult) female spiders that fed HL flies matured with significantly higher lipid content than those fed LL flies. We found that the mated females fed with HL flies significantly shortened pre-oviposition time and resulted in a significantly higher fecundity. However, there was no significant difference in female spiders varying in lipid content on other behaviors and traits, including the latency to courtship, courtship duration, mating, copulation duration, sexual cannibalism, offspring body size and survival. Hence, our results suggest that the lipid content of prey may be a limiting factor for female reproduction, but not for other behavioral traits in the wolf spiders P. pseudoannulata.
Anthropocentrism and the perceived great dissimilarity of these animals compared to humans also help to explain the lack of concern, aversion, and even fear with which many people regard invertebrates. Concerns for animal welfare in vertebrate livestock production are similar to those for invertebrate production, especially when practiced on a large scale. Resources for information on invertebrate animal husbandry, biology, and medicine are listed in the "Recommended Reading" section. Invertebrate cognitive function is often thought to be limited, resulting in behavioral repertoires consisting primarily of reflexes or preprogrammed patterns. Invertebrates display other intriguing actions in response to stimuli that are believed to cause pain in vertebrate species. Physiological evidence for pain in invertebrates lies primarily with aspects of their neurochemical systems. Euthanasia of any animal should be performed humanely, manifested by providing for minimal pain and distress. A common practice among scientists for invertebrate specimen collection is submersion in a preservative substance.
Full-text available
The central nervous system is known to be plastic in volume and structure depending on the stimuli the organism is subjected to. We tested in the jumping spider Marpissa muscosa (Clerck, 1757), whether rearing environments affect the volume of two target higher-order brain centers: the mushroom body (MB) and the arcuate body (AB). We reared female M. muscosa (N = 39) in three environments: solitarily (D: deprived), solitarily but in a physically enriched environment (P: physically enriched) and together with several siblings (G: group). We additionally investigated spiders caught from the field (W: wild). Volumes of MB and AB were compared using microCT analysis. We hypothesized that spiders reared in treatments P and G should have larger MB and AB than the spiders from treatment D, as the enriched environments are presumably cognitively more demanding than the deprived environment. Spiders from treatment P had significantly larger absolute brain volumes than spiders from treatment D, whereas brain volumes of treatment G lay in between. The relative volume of the MB was not significantly different between the treatments, whereas relative AB volumes were significantly larger in treatment P than in D, supporting the hypothesis that the AB is a center of locomotor control. W spiders had smaller absolute brain volumes and relatively smaller AB than spiders from laboratory treatments, which suggests developmental constraints under natural, possibly food-limited conditions. Additionally, differences in the relative volume of MB substructures were found. Overall, our study demonstrates that brains of jumping spiders respond plastically to environmental conditions in that absolute brain volume, as well as the relative volume of higher-order brain centers, is affected.
Full-text available
Mate choice decisions are central in sexual selection theory aimed to understand how sexual traits evolve and their role in evolutionary diversification. We test the hypothesis that brain size and cognitive ability are important for accurate assessment of partner quality and that variation in brain size and cognitive ability underlies variation in mate choice. We compared sexual preference in guppy female lines selected for divergence in relative brain size, which we have previously shown to have substantial differences in cognitive ability. In a dichotomous choice test, large-brained and wild-type females showed strong preference for males with color traits that predict attractiveness in this species. In contrast, small-brained females showed no preference for males with these traits. In-depth analysis of optomotor response to color cues and gene expression of key opsins in the eye revealed that the observed differences were not due to differences in visual perception of color, indicating that differences in the ability to process indicators of attractiveness are responsible. We thus provide the first experimental support that individual variation in brain size affects mate choice decisions and conclude that differences in cognitive ability may be an important underlying mechanism behind variation in female mate choice.
Full-text available
Spiders have been suspected to be one of the most important groups of natural enemies of insects worldwide. To document the impact of the global spider community as insect predators, we present estimates of the biomass of annually killed insect prey. Our estimates assessed with two different methods suggest that the annual prey kill of the global spider community is in the range of 400–800 million metric tons (fresh weight), with insects and collembolans composing >90% of the captured prey. This equals approximately 1‰ of the global terrestrial net primary production. Spiders associated with forests and grasslands account for >95% of the annual prey kill of the global spider community, whereas spiders in other habitats are rather insignificant contributors over a full year. The spider communities associated with annual crops contribute less than 2% to the global annual prey kill. This, however, can be partly explained by the fact that annual crop fields are “disturbed habitats” with a low buildup of spider biomass and that agrobiont spiders often only kill prey over short time periods in a year. Our estimates are supported by the published results of exclusion experiments, showing that the number of herbivorous/detritivorous insects and collembolans increased significantly after spider removal from experimental plots. The presented estimates of the global annual prey kill and the relative contribution of spider predation in different biomes improve the general understanding of spider ecology and provide a first assessment of the global impact of this very important predator group.
Full-text available
There is a tension between the conception of cognition as a central nervous system (CNS) process and a view of cognition as extending towards the body or the contiguous environment. The centralised conception requires large or complex nervous systems to cope with complex environments. Conversely, the extended conception involves the outsourcing of information processing to the body or environment, thus making fewer demands on the processing power of the CNS. The evolution of extended cognition should be particularly favoured among small, generalist predators such as spiders, and here, we review the literature to evaluate the fit of empirical data with these contrasting models of cognition. Spiders do not seem to be cognitively limited, displaying a large diversity of learning processes, from habituation to contextual learning, including a sense of numerosity. To tease apart the central from the extended cognition, we apply the mutual manipulability criterion, testing the existence of reciprocal causal links between the putative elements of the system. We conclude that the web threads and configurations are integral parts of the cognitive systems. The extension of cognition to the web helps to explain some puzzling features of spider behaviour and seems to promote evolvability within the group, enhancing innovation through cognitive connectivity to variable habitat features. Graded changes in relative brain size could also be explained by outsourcing information processing to environmental features. More generally, niche-constructed structures emerge as prime candidates for extending animal cognition, generating the selective pressures that help to shape the evolving cognitive system.
Full-text available
The euthanasia of invertebrates used in scientific investigations poses unanswered questions regarding the rapid induction of unconsciousness with minimal distress and pain. Relative to vertebrates, invertebrates' sensory experience of pain, nociception, and physiologic response to aversive stimuli are poorly characterized. The scientific communities in the European Union, Canada, United States, Australia, and New Zealand join in consensus regarding the need to address alleviation of pain and distress in cephalopods (octopus, squid, and so forth), which have the best-characterized nervous system among invertebrates. In the current study, we evaluated various euthanasia techniques in a terrestrial gastropod species, with priority on animal wellbeing, scientific variability, feasibility in both field and laboratory settings, and acceptability by personnel. In addition, we demonstrated that the 2-step method of euthanasia described in the AVMA Guidelines as acceptable for aquatic invertebrates is effective for terrestrial snails and meets all welfare and scientific requirements. This 2-step method first induces anesthesia by immersion in 5% ethanol (laboratory-grade ethanol or beer) followed by immersion in a euthanizing and tissue-preserving solution of 70% to 95% ethanol or 10% neutral buffered formalin. Furthermore, alternative methods of euthanasia for terrestrial snails commonly used in field research, such as live immersion in concentrated ethanol or formalin, were shown to be unacceptable. Copyright 2016 by the American Association for Laboratory Animal Science.
Jumping spiders are known for their extraordinary cognitive abilities. The underlying nervous system structures, however, are largely unknown. Here, we explore and describe the anatomy of the brain in the jumping spider Marpissa muscosa (Clerck, 1757) by means of paraffin histology, X-ray microCT analysis and immunohistochemistry as well as three-dimensional reconstruction. In the prosoma, the CNS is a clearly demarcated mass that surrounds the esophagus. The anteriormost neuromere, the protocerebrum, comprises nine bilaterally paired neuropils, including the mushroom bodies and one unpaired midline neuropil, the arcuate body. Further ventrally, the synganglion comprises the cheliceral (deutocerebrum) and pedipalpal neuropils (tritocerebrum). Synapsin-immunoreactivity in all neuropils is generally strong, while allatostatin-immunoreactivity is mostly present in association with the arcuate body and the stomodeal bridge. The most prominent neuropils in the spider brain, the mushroom bodies and the arcuate body, were suggested to be higher integrating centers of the arthropod brain. The mushroom body in M. muscosa is connected to first and second order visual neuropils of the lateral eyes, and the arcuate body to the second order neuropils of the anterior median eyes (primary eyes) through a visual tract. The connection of both, visual neuropils and eyes and arcuate body, as well as their large size corroborates the hypothesis that these neuropils play an important role in cognition and locomotion control of jumping spiders. In addition, we show that the architecture of the brain of M. muscosa and some previously investigated salticids differs significantly from that of the wandering spider Cupiennius salei, especially with regard to structure and arrangement of visual neuropils and mushroom body. Thus, we need to explore the anatomical conformities and specificities of the brains of different spider taxa in order to understand evolutionary transformations of the arthropod brain.
Invertebrate Medicine, Second Edition offers a thorough update to the most comprehensive book on invertebrate husbandry and veterinary care. Including pertinent biological data for invertebrate species, the book's emphasis is on providing state-of-the-art information on medicine and the clinical condition. Invertebrate Medicine, Second Edition is an invaluable guide to the medical care of both captive and wild invertebrate animals. Coverage includes sponges, jellyfish, anemones, corals, mollusks, starfish, sea urchins, crabs, crayfish, lobsters, shrimp, hermit crabs, spiders, scorpions, and many more, with chapters organized by taxonomy. New chapters provide information on reef systems, honeybees, butterfly houses, conservation, welfare, and sources of invertebrates and supplies. Invertebrate Medicine, Second Edition is an essential resource for veterinarians in zoo animal, exotic animal and laboratory animal medicine; public and private aquarists; and aquaculturists.
Spiders are often underestimated as suitable behavioural models because of the general belief that due to their small brains their behaviour is innate and mostly invariable. Challenging this assumption, this fascinating book shows that rather than having a limited behavioural repertoire, spiders show surprising cognitive abilities, changing their behaviour to suit their situational needs. The team of authors unravels the considerable intra-specific as well as intra-individual variability and plasticity in different behaviours ranging from foraging and web building to communication and courtship. An introductory chapter on spider biology, systematics and evolution provides the reader with the necessary background information to understand the discussed behaviours and helps to place them into an evolutionary context. Highlighting an under-explored area of behaviour, this book will provide new ideas for behavioural researchers and students unfamiliar with spiders as well as a valuable resource for those already working in this intriguing field.