Exploration behaviour and behavioural flexibility in orb

Current Zoology
61 (2): 313–327, 2015
Exploration behaviour and behavioural flexibility in
orb-web spiders: A review
Thomas HESSELBERG*
Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK
Abstract Orb-web spiders and their webs constitute an ideal model system in which to study behavioural flexibility and spatial
cognition in invertebrates due to the easily quantifiable nature of the orb web. A large number of studies demonstrate how spiders
are able to modify the geometry of their webs in response to a range of different conditions including the ability to adapt their
webs to spatial constraints. However, the mechanisms behind this impressive web-building flexibility in these cognitively limited
animals remain poorly explored. One possible mechanism though may be spatial learning during the spiders’ exploration of their
immediate surroundings. This review discusses the importance of exploration behaviour, the reliance on simple behavioural rules,
and the use of already laid threads as guidelines for web-building in orb-web spiders. The focus is on the spiders’ ability to detect
and adapt their webs to space limitations and other spatial disruptions. I will also review the few published studies on how spatial
information is gathered during the exploration phase and discuss the possibility of the use of ‘cognitive map’-like processes in
spiders. Finally, the review provides suggestions for designing experimental studies to shed light on whether spiders gather metric
information during the site exploration (cognitive map hypothesis) or rely on more simple binary information in combination
with previously laid threads to build their webs (stigmergy hypothesis) [Current Zoology 61 (2): 313–327, 2015].
Keywords
1
Animal cognition, Spider web-building, Stigmergy, Cognitive maps, Exploration behaviour, Behavioural plasticity
Introduction
1.1 Spatial cognition and cognitive maps
The ability to sense and gain knowledge of the local
physical environment is a requirement for survival in
most animal species. The immediate surroundings provide a source of food, mating opportunities and other
resources such as shelter, building materials and direction cues, but is also where predators might arrive from.
Thus formation of a coherent picture of the local habitat
is adaptive for a wide range of animals. Spatial cognition is defined as the ability to gather and learn spatial
information of directions and distances. However, our
understanding of spatial cognition remains poorly explored, although the processing of spatial information
and learning appears to have different computational
requirements than temporal associative learning (Shettleworth, 2010). Most of what we know about spatial
cognition relates to navigation and orientation. Much
orientation and short-distance navigation is based on
less cognitive demanding abilities such as auditory, light,
chemical and pheromone gradients, path integration and
ideothetic memory, while long-distance navigation requires the ability to integrate, and prioritise among,
Received Nov. 1, 2014; accepted Feb. 5, 2015.
 Corresponding author. E-mail: [email protected]
© 2015 Current Zoology
multiple cues and abilities such as the use of visual
landmarks, polarised light and magnetic gradients in
addition to the above mentioned abilities (Mouritsen,
2001; Frost and Mouritsen, 2006; Shettleworth, 2010).
However, the most computational demanding, but also
most controversial, aspect of spatial cognition is the
ability to form a map-like representation of the environment. This concept is known as cognitive maps,
which are defined as the ability to learn metric properties of space, i.e. distances and directions, and perform
mental operations on the learned properties to follow
novel routes to well-known locations (Tolman, 1948;
Shettleworth, 2010).
The concept of cognitive maps was first defined by
Tolman (1948), who studied rats’ problem solving ability in mazes. He found that they learn and store spatial
relationships of their surroundings in a field map, which
is distinct from, and more complicated than, forming
simple sequential stimulus response connections of the
correct path through a maze. Since his seminal studies,
cognitive maps and the ability to remember relations
between geometrical landmarks have been found in a
number of visually orientating vertebrates (see Tommasi
et al., 2012 for a review). The idea that invertebrates
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possess a cognitive map that allow them to judge distances and directions between geographically separate
points has been discussed for some time particular in
relation to navigation in social insects. Several authors
have argued that honey bees are capable of making
novel short cuts in a familiar habitat and thus may possess a spatial memory of their surroundings akin to a
cognitive map based on previous exploratory flight experience (Gould, 1986; Menzel et al., 2005). However,
another theoretical study on neural networks in desert
ants suggests that such novel short cuts can be explained by separate decentralised memory subsystems
relying on landmark guidance and path integration without the need to postulate a centralised spatial memory
system that relies on cognitive maps (Cruse and Wehner,
2011). In contrast, a very recent study found that honey
bees with shifted sun-compass caused by anesthesia
readily orient towards home (Cheeseman et al., 2014a),
which the authors interpret as a proof of the honeybees’
possession of cognitive maps, although their interpretation has been questioned (Cheung et al., 2014; Cheeseman et al., 2014b). Thus despite a relatively large number of studies, there is still no clear consensus as to
whether insects possess a cognitive map or not. We
know even less about spatial cognition in other invertebrates although spiny lobsters are proposed to employ a
magnetic map for navigation (Boles and Lohmann,
2003). Spiders usually do not need to make longdistance journeys to and from fixed locations and thus
do not engage in complicated navigation tasks with a
few exceptions; the jumping spider Portia fimbriata is
capable of making detours that temporarily involves it
moving away from the target prey (Tarsitano and Jackson, 1992; Jackson and Pollard, 1996) and the males of
the desert huntsman spider Leucorchestris arenicola
make long nocturnal journeys searching for females
while usually returning to their burrows in a straight
line after each journey probably by relying on a combination of path integration and local cues (Nørgaard et al.,
2003; 2007). Nonetheless navigation is not the only task
where possessing a cognitive map might be advantageous. Web-building spiders assess the suitability of a
site for their webs based on prior exploration (Vollrath,
1992).
1.2 Web-building behaviour and orb-web spiders
Web-building spiders in general and orb-web spiders
in particular are excellent model organisms for studies
of cognitive abilities in terrestrial non-insect invertebrates since they leave a physical record, i.e. the web, of
their foraging behaviour (Vollrath and Selden, 2007).
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Orb webs are furthermore highly regular geometric twodimensional structures, which make them easily quantifiable. The typical orb web consists of a hub from which
radii radiate outwards towards the frame which is connected to the surrounding vegetation via anchor threads
(Fig. 1). Enclosed within the frame and connected to the
radii is the sticky capture spiral which functions to trap
intercepted prey long enough for the spider to rush out
from the hub to catch them (Eberhard, 1990a). The spiders are usually resting motionless in the hub or on
nearby vegetation while connected to the hub through a
signal thread from where they will initiate prey attack
behaviour when vibratory signals from the struggling
prey reach the hub via the radii (Masters et al., 1986;
Landolfa and Barth, 1996). In most webs, the hub is not
located in the exact centre of the web, but usually displaced upwards to give asymmetric webs with a larger
lower part reflecting the fact that spiders, due to gravity,
can run faster downwards than upwards (Fig. 1; ap Rhiziart and Vollrath, 1994; Zschokke and Nakata, 2010).
Almost 4,500 species of orb-web spiders are known
from all continents, except Antarctica, belonging to 7
families (Anapidae, Araneidae, Nephilidae, Symphytognathidae, Theridisomatidae, Tetragnathidae and Uloboridae). Some spiders include a missing sector in the
corner of the web, where a signal thread runs from the
hub to the spider’s retreat in the nearby vegetation, while
many spiders that always reside in the hub include web
Fig. 1 An orb web of Cyclosa caroli digitised from a photograph
The figure shows the anchor threads (Anc) that connects the web to
the surrounding vegetation, the radii (Rad) radiate outwards from the
hub in the centre of the web until they reach the frame (Fr). The sticky
capture spiral (Cap) is connected to the radii.
HESSELBERG T: Exploration behaviour in orb-web spiders
decorations made of silk or prey remains and debris
primarily used to camouflage the spiders or attract prey
(Herberstein et al., 2000a; Bruce, 2006; Nakata, 2009;
Walter and Elgar, 2012). Further advantages of using
orb-web spiders as model organism for cognitive studies
include that most orb-web spiders readily built webs in
frames under laboratory conditions (Zschokke and Herberstein, 2005) and that they are highly motivated to
build webs even under adverse physiological and environmental conditions such as when missing legs (Reed
et al., 1965; Pasquet et al., 2011), when under the influence of pesticides and neurotoxic drugs (Witt, 1971;
Samu and Vollrath, 1992; Hesselberg and Vollrath, 2004;
Benamú et al., 2010; 2013), when exposed to space limitations (Ades, 1986; Vollrath et al., 1997; Barrantes
and Eberhard, 2012; Hesselberg, 2013) and when exposed to weightlessness in space (Witt et al., 1977).
Once the site has been found to be suitable, orb-web
spiders construct their webs in four more or less stereotypical phases. In phases I and II, which is covered in
more detail later, they identify the location of the web,
build the radii, frame and anchor threads. In phase III
they construct the auxiliary spiral (also known as the
temporary or non-sticky spiral) that starts at the hub and
logarithmically spirals outwards, where it mechanically
stabilises the scaffolding structure of the web and,
among other cues, acts as a guideline for the construction of the sticky spiral (Peters, 1970; Zschokke, 1993;
2011; Eberhard and Hesselberg, 2012). The auxiliary
spiral is usually removed during construction of the
sticky spiral although some members of the Nephilidae
family retain it in the intact web, presumably to strengthen the web (Kuntner and Agnarsson, 2009; Hesselberg
and Vollrath, 2012). In contrast, miniature orb-web
spiders in the Anapidae family do not build auxiliary
spirals at all (Eberhard, 1987a). Phase IV takes the
longest for the spider to finish and is where the geometric capture spiral is constructed. The spider starts from
the near the frame and build towards the hub attaching
each spiral loop to every radius that it crosses. The capture spiral is built as a geometric spiral ensuring that the
distance between the spiral loops is more or less regular
across the web (although see Eberhard, 2014).
Numerous studies have investigated web-building
behaviour and the geometry of the completed web in
detail under a wide variety of environmental and physiological conditions revealing a surprisingly degree of
behavioural flexibility as we shall see in the next section. However, we know next to nothing about the exploration behaviour preceding the onset of the web-buil-
315
ding behaviour. In this paper, I first review some examples of remarkable cognitive abilities in orb-web spiders
including behavioural flexibility and learning. In the
following section I go into details with what we know
about the exploration behaviour and the early web
building behaviour while discussing the implications for
spatial cognition in orb-web spiders. The review builds
on Vollrath’s excellent review paper (Vollrath, 1992) on
exploration and web-building behaviour, which first
discussed the possibility that orb-web spiders may construct spatial maps. I therefore focus especially on studies conducted after 1992 as well as linking spatial cognition more explicitly to neuroethology and behavioural
flexibility. In the final section, I introduce two extreme
hypotheses in terms of cognitive demand; the stigmergy
and the cognitive map hypotheses, discuss and evaluate
their predictions, present some preliminary data and
suggest further experiments that might shed light on the
type of information obtained by the spiders during their
exploration behaviour.
2 Cognition, Behavioural Flexibility
and Spatial Constraints
2.1 The spider brain and behavioural limitations
Given the current and historic fascination of spider
webs and spider web-building behaviour from both scientists and lay people, we know surprisingly little about
the underlying cognitive processes. The central nervous
system of orb-web spiders, like that of all spiders, consists of two compact ganglia; the subesophageal and the
supraesophageal ganglion (Foelix, 2011). The subesophageal ganglion, which as the name implies is located
below the esophagus, is the main centre for linking
sensory input to motor output and consists of the fused
ganglia of the appendages. The supraesophageal ganglion, also referred to as the ‘brain’, is the most complex part of the central nervous system and consists of
several different structures including the protocerebrum,
which contains the central body, and the optic nerves
(Babu, 1975; Park et al., 2013). As the supraesophageal
ganglion receives sensory input from the eyes, it is most
highly developed in spiders with good vision such as
jumping spiders and wolf spiders (Foelix, 2011). Orbweb spiders on the other hand have poor vision and can
build perfectly normal orb webs in total darkness and
instead primarily rely on mechanosensory cues for building their webs and capturing their prey (Spronk, 1935;
Land, 1985; Foelix, 2011). Although their supraesophageal ganglion is not as complex as in some other
spiders, it has (and the central body in particular) none-
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theless attracted much attention in connection with webbuilding behaviour. Volumetric measurements, however,
failed to find any differences in relative size of the central body between the orb-web spider Nephila clavipes
and three web-less spiders (Weltzien and Barth, 1991).
Nonetheless, the central body remains at present the
most likely candidate for the brain structure that governs web-building behaviour (Park et al., 2013). This is
supported by older studies on the orb-web spider Araneus diadematus displaying disruption to normal webbuilding behaviour after its protocerebrum was damaged with laser light (Witt and Reed, 1964; Witt, 1969).
Since there appears to be no large differences between the central nervous system of adult web-building
and web-less spiders, perhaps the cognitive demands of
web-building can instead best be explored by comparing the webs of early instar and adult spiders. The size
limitation hypothesis proposes that early instar juveniles,
which can be up to 1,000 times smaller than the adults
(Eberhard, 2011; Hesselberg, 2010), should, due to their
resultant miniature brains, be less precise, more behaviourally limited or commit more errors during webbuilding than adults. However, three experimental studies comparing early instar juveniles and adults of four
species of orb-web spiders fail to provide any support
for this hypothesis (Eberhard, 2007; Hesselberg, 2010;
Eberhard, 2011). Although this can partly be explained
by early instar spiders enlarging their central nervous
system by expanding it into their legs (Quesada et al.,
2011), the failure to find any kind of behavioural differences, and the findings that other non-web-building
kleptoparasitic spiders show a similar brain enlargement
in early instars (Quesada et al., 2011) supports the conclusion from the neurophysiological studies that webbuilding behaviour is achieved by following relatively
simple rules based on guidance from previously laid
threads (Peters, 1939; Zschokke, 1993; 2011; Eberhard
and Hesselberg, 2012). This is further supported by
computer models of web-building behaviour that while
following a few simple rules successfully simulate completed webs built by both normal spiders (Krink and
Vollrath, 1998) and by spiders with shorter regenerated
front legs (Krink and Vollrath, 1999).
2.2 Learning and memory
As we saw above, juvenile spiders do not commit
more errors than adult spiders, but do early instar spiders build perfect webs from the start or do they improve
their web-building behaviour through practice? The acquisition of complex motor skills through experience is
well known from humans and other vertebrates, but
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there is also growing evidence that motor learning and
plasticity may be widespread in invertebrates (Chittka
and Niven, 2009; Wolf et al., 1992). Bees for instance
learn specific motor sequences while foraging in a
complex artificial environment (Collett et al., 1993) and
fruit flies, without prior flight experience, show less
precise steering control compared to more experienced
flies (Hesselberg and Lehmann, 2009). However, a
study of spider web-building behaviour revealed no differences in web geometry between inexperienced and
experienced spiders (Reed et al., 1970). In general orbweb spiders do not seem to improve their web-building
skills with experience and show no major differences in
web geometry throughout life (Pasquet et al., 2014),
except that old spiders build webs that contain more
errors (Anotaux et al., 2012). However, some minor
differences are found in that older heavier, spiders build
more vertically asymmetric webs, although this difference is likely caused by older spiders also being heavier
(Herberstein and Heiling, 1999; Venner et al., 2013;
Hesselberg, 2010; Nakata, 2010; Kuntner et al., 2010;
Gregoric, 2013) and that early instar juveniles of species that as adults include a free sector often build webs
without a free sector (Hesselberg, 2010). Although webbuilding behaviour in spiders appears to be innate, this
does not mean that they do not show learning in other
aspects. The golden orb-web spider Nephila clavipes
has recently been shown to remember the amount (and
possibly the number) of recently caught and stored prey
(Rodríguez et al., 2013; 2014), the trashline orb-web
spider Cyclosa octotuberculata learns the spatial location of recently caught prey in the web and selectively
pulls radii in that sector (Nakata, 2013), and the missing
sector orb-web spider Zygiella x-notata has been shown
to rely on memory of the direction to its retreat when
returning from excursions onto the web (LeGuelte,
1969). Evidence furthermore suggests that spiders rely
on memory of distances travelled and the location of
previously laid spiral threads during construction of the
auxiliary and capture spirals (Eberhard, 1988a; Eberhard and Hesselberg, 2012). Finally, orb-web spiders
modify the geometry of their webs based on the type
and size of previously caught prey (Schneider and Vollrath, 1998; Venner et al., 2000; Tso et al., 2007; Blamires et al., 2011) and also on the presence of potential
prey in their environment (Pasquet et al., 1994).
2.3 Behavioural flexibility and cognitive abilities
Notwithstanding the examples of learning discussed
above, one of the orb-web spiders’ most impressive
cognitive abilities is probably their extensive beha-
HESSELBERG T: Exploration behaviour in orb-web spiders
vioural flexibility when it comes to the size, shape and
geometry of their webs. A very wide range of environmental and physiological factors affect the completed
orb webs, but we need to separate factors that limit the
spider’s ability to construct normal webs (i.e. factors
that induce errors) from factors that result in adaptive
changes to the web as a result of behavioural flexibility
(i.e. factors that result in modified webs that are better
adapted to a given situation). However, it is not always
easy to make this distinction. While some changes to
orb web geometry are clearly non-adaptive such as
those caused by neurotoxins and pesticides (Witt, 1971;
Samu and Vollrath, 1992; Hesselberg and Vollrath, 2004;
Benamú et al., 2010; 2013), by old age (Anotaux et al.,
2012) and by ectoparasites (Eberhard, 2000; 2010; Gonzago and Sobzcak, 2011), others are less straightforward.
Rotating the frame while spiders are building their webs,
for example, results in suboptimal webs probably due to
disruption to the gravitational cue (Vollrath, 1986;
1988), but at higher rotations webs become more normal suggesting that the spider shifts to rely on centripetal forces instead which confirms the findings of earlier studies that spiders in space apparently can modify
their use of gravitational cues (Witt et al., 1977). Similarly humidity seems to influence the orb web by reducing its size and minimising the distance between
spiral turns at lower humidity (Vollrath et al., 1997),
which could be an adaptation to the reduced stickiness
of the capture spiral threads at lower humidity (Edmonds and Vollrath, 1992; Opell et al., 2011). Losing
one or several legs also affect geometry of the web
(Pasquet et al. 2011), but this constitute a more obvious
example of adaptation, since all legs normally play a
Fig. 2
317
role during web-building (Reed et al., 1965; Vollrath,
1987; Eberhard, 1990b; 2012), so the construction of
functional webs, even when missing 2‒4 legs (T. Hesselberg, Pers. Obs.), suggests a high degree of plasticity
in the construction rules. Clear examples of behavioural
flexibility additionally include the matching of size and
geometry to the available silk supply (Eberhard, 1988b),
the increase in the distance between capture spiral turns
at lower temperatures to decrease web-building time
and/or to better target the larger insects still active (Vollrath et al., 1997) and the decrease in web size and overall thread length and increase in stiffness and distance
between spiral turns that reduces drag in wind-exposed
webs (Vollrath et al., 1997; Liao et al., 2009; Wu et al.,
2013).
One of the most striking examples of adaptive behavioural flexibility, however, is some orb-web spiders’
ability to adapt the size and shape of their webs to spatial constraints in the space available for building their
webs in (Fig. 2). Some, but not all, orb-web spiders readily build webs in limited spaces with less than a fourth
of the area of their normal webs in the field (Vollrath et
al., 1997; Hesselberg, 2013), with Leucauge argyra
even building in containers that allow only webs less
than a tenth of the size in the field (Barrantes and Eberhard, 2012), while also vertically or horizontally elongating the shape of their webs to match the available space
(Vollrath et al., 1997; Krink and Vollrath, 2000; Harmer
and Herberstein, 2009; Harmer et al., 2012; Hesselberg,
2013). Interestingly, though this and the previously described examples of web-building flexibility all appear
to be examples of activational behavioural plasticity,
which is defined as an immediate response that relies on
Webs built by Eustala illicita in experimental frames in the laboratory
The highlighted black spirals show the location and shape of the auxiliary spiral reconstructed from silk remnants left in the completed web. A.
Webs built in control frames show the normal shape and geometry. B. Webs built in vertical frames show significantly vertically elongated webs. C.
Webs built in horizontal frames show significantly horizontally elongated webs. D. Webs built in small square frames show smaller but normal
shaped and slightly compressed webs. E. The size of the experimental Perspex frames in which the spiders built their webs. All measurements are in
cm and all frames were 5 cm wide. The white horizontal scale bars represent a length of 5 cm. Figure from Hesselberg (2013) with kind permission
from Springer Science+Business Media.
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Current Zoology
pre-configured neural pathways rather than developmental behavioural plasticity that relies on modification
of neural pathways through learning from experience
(Snell-Rood, 2013; Hesselberg, 2014). Thus spiders
tested in the experimental frames in Fig. 2 showed an
immediate adaptation to the frames and did not improve
their shape or area utilisation in subsequent webs build
in the same frames (Hesselberg, 2014).
3
Exploration Behaviour, Construction
of Attachments Points and Anchor
Threads
3.1 Exploration behaviour
In the previous section we learned that the present
evidence supports the notion that despite the structural
complexity of orb webs, their construction requires no
more cognitive abilities than any other foraging behaviour and possibly significantly less than other specialised invertebrate behaviours. Therefore in order to explore the cognitive demands of web-building and search
for the potential use of cognitive maps, we should instead focus on the behaviour that precedes the more
stereotypical radial and spiral construction behaviour.
As mentioned in the introduction we can divide the
web-building behaviour into four more or less distinct
stages (exploration, frame and radii construction, temporary spiral construction and capture spiral construction). The exploration behaviour stage is the one we
know the least about and the little we do know comes
from laboratory studies, where webs are built in a much
more limited and structurally simpler space than in nature (Eberhard, 1972; Zschokke, 1996). The function of
site exploration is probably to assess if the site contains
large enough unobstructed space for the construction of
a web and to determine the potential attachment points
of the anchor threads that connects the finished web
with the vegetation (Ebehard, 1972; Vollrath, 1992). Orbweb spiders have very poor eyesight (Spronk, 1935;
Land, 1985; Foelix, 2011), so such as an assessment
must rely on other sensory cababilities. There is some
evidence that spiders associated with specific plant species could use chemical signals to determine the suitability of a site (Krell and Krämer, 1998; Romero et al.,
2008; Hesselberg and Triana, 2010; Styrsky, 2014) and
spiders may also assess the quality in terms of foraging
potential by picking up vibrations transmitted through
the air by flying insects (Pasquet et al., 1994; Herberstein et al., 2000b). However, in order determine the suitability of the space for constructing a web, the spiders
Vol. 61 No. 2
need to physically explore the vegetation. In nature
spiders probably rely on a combination of walking
around and using airborne lines to traverse gaps in the
vegetation (Vollrath, 1992; Foelix, 2011). Spiders release silk into the air from their spinnerets by raising
their abdomen or by descending a silk thread, which
ensures that wind will carry the light and fluffy threads
to nearby vegetation (Eberhard, 1987b; Peters, 1990).
Once the airborne thread has attached itself the spider
will tighten the thread and walk across it while replacing it with stronger silk. In the absence of wind in the
laboratory (and with the much smaller distances involved), spiders move around the edges of the frame of
the cage continuously trailing silk threads (Fig. 3;
Eberhard, 1972; Vollrath, 1992; Zschokke, 1996). Spiders building vertical webs will then often move along
horizontal threads in the upper part of the frame while
occasionally descending vertically until they reach the
ground upon which they double back (Fig. 3; Eberhard,
1990b; Zschokke, 1996). The function of this behaviour
could be to ensure that the space is free of obstacles and
is therefore probably also found during web-building in
nature. The problem with observing exploration behaviour in the wild is that it often takes place several
hours before the actual web construction starts and the
exploration behaviour often consists of short periods of
activity followed by long periods of inactivity (Eberhard, 1972; 1990b) making it virtually impossible to
recognise it as exploration behaviour before actual webbuilding commences. However, an exception is a study
on the complete web-building sequence in the wild of
the Darwin’s bark spider (Gregorič et al., 2011). The
Darwin’s bark spider builds large webs spanning rivers
with anchor thread lengths often exceeding 10 m. It
crosses the river by releasing silk threads into the wind
as described above, but interestingly once it has established a silk thread across the river, it builds its web
directly underneath this initial thread over the middle of
the river with only one further long anchor thread below
the web attaching it to one of the river banks (Gregorič
et al., 2011). This species does not appear to perform
any further site exploration once the initial river spanning silk thread is established. The Darwin bark’s spider
probably gets away with drastically reducing the exploration stage since spaces above water bodies are usually
free of any obstacles and since the use of only three
anchor points automatically ensures that the web is built
in one plane (Gregorič et al., 2011). In general, it is important to note that although site exploration only takes
place when spiders relocate to a new location or com-
HESSELBERG T: Exploration behaviour in orb-web spiders
pletely lose their webs due to wind or other disturbances
(Zschokke, 1996; Wherry, 2009), the fitness consequences of selecting a high-quality web site are so significant that we would expect natural selection to have optimised this behaviour. Usually spiders take down their
old webs by ingesting the silk threads and recycling the
proteins before rebuilding a new web at the same site
without displaying exploration behaviour and reusing at
least some of the anchor threads from the previous web
(Breed et al., 1954; Peakall, 1971; Zschokke, 1996;
Zschokke and Vollrath, 2000).
3.2 Early stages of web construction
Once the site is found acceptable for web-building
(the exact mechanism for how the spider does this is
unknown, but I will discuss a few potential mechanisms
in the next section), the spider starts, after a period of
time, to construct the web. During exploration the spider, by trailing its dragline, has left some threads crisscrossing the free space and the spider uses the intersection of these threads as a proto-hub to add radii from
(Zschokke, 1996). This first simple structure sometimes
takes the form of a Y (Peters, 1937; 1939; Foelix, 2011),
but can also consists of 4-7 protoradii running from the
surrounding vegetation or structure and meeting in the
proto-hub (Zschokke and Vollrath, 1995; Zschokke,
1996). The spider then starts to build the frame in the
upper part of the web sometimes removing previous
threads and constructing new anchor threads before it
moves the proto-hub by cutting and reattaching the
proto-radii into a new (usually more central) position
that then becomes the hub (Eberhard, 1990b; Zschokke
and Vollrath, 1995; Zschokke, 1996). This is followed
by the addition of a few more radii in different sections
of the web as well as simultaneously finishing the construction of the frame and finalising the position of the
Fig. 3 The tracks of an Araneus diadematus spider showing the exploration behaviour of two subsequent webs
built in the laboratory
Tracks were recorded with computer-automated tracking software.
In the first web (A) the spider spent less time exploring than during
the second web (B). The vertical descents are visible in both figures,
but especially during the exploration prior to the second web (B).
Figure from Zschokke (1996) with kind permission from the Museum
of Natural History in Geneva and the Swiss Zoological Society.
319
anchor threads. During this process the spider attempts
to keep the structure in one plane by usually, although
not always, attaching the anchor threads within the
same plane (Zschokke and Vollrath, 2000). It is important to keep the web as much as possible in one plane,
since this ensures the largest possible projection area
(and thus effective capture area) per web area and distribute the forces from prey impact and wind more
equally (Wainwright et al., 1976; Denny, 1976; Lin et
al., 1995). After the frame has been completed the spider builds the remaining radii by identifying large gaps
between existing radii and then moving out along an
existing radius (the exit radius) and some distance down
the frame where it attaches the trailing dragline to the
frame and moves along this new radius back to the hub
(Eberhard, 1990; Zschokke, 1996). A preliminary study
suggests that the exact distance moved on the frame,
and thus the attachment point for the new radius, might
be determined by the spider relying on path integration
to locate the direction to the hub (Vollrath et al., 2002).
During this process the new radius is usually placed
immediately below the exit radius and gaps are filled in
alternate sections of the web, presumably to ensure
mechanical stability of the structure during construction
(Wirth and Barth, 1992; Zschokke, 1996). Once all gaps
have been filled the spider strengthens the hub before
building the auxiliary spiral and the capture spiral. In
some species additional radii are sometimes added to
the structure during the construction of the auxiliary
spiral (Zschokke and Vollrath, 1995)
4
Cognitive Maps, Preliminary Studies
and Suggestions for Further
Experiments
In the previous section we saw how spiders obtain
essential information on the quality of a potential webbuilding site through exploration. To successfully determine if a web should be build, the spider requires
information on i) the size of the available space and the
presence (and potentially the location) of suitable anchoring points in the surrounding vegetation and ii)
whether the available space is free of obstructions or not.
There are several ways that such information can theoretically be obtained varying in the cognitive demands
made on the spider brain. Below I outline two extremes;
the cognitively very demanding spatial awareness and
cognitive map hypothesis (from now on referred to as
the cognitive map hypothesis) and the much less cognitively demanding binary information and stigmergy hy-
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pothesis (from now on referred to as the stigmergy hypothesis), before I discuss their predictions and evaluate
the admittedly limited evidence for and against them.
4.1 The cognitive map hypothesis
The cognitive map hypothesis proposes that spiders
construct some form of metric map during site exploration providing information on the size and shape of
available space as well as possibly on the location and
direction of potential anchor thread attachment points.
The potential use and nature of cognitive maps in the
practically blind orb-web spiders would though be different from the cognitive maps we discussed earlier
used for navigation in visually orientated animals. There
is relatively limited evidence for the generation of nonvisual spatial maps and for non-visual navigation in
general among animals. However, bats are known to use
acoustic landmarks in orientation (Jensen et al., 2005)
and the ability to generate olfactory spatial maps are
proposed to exist in both vertebrates and invertebrates
(Jacobs, 2012). Furthermore, magnetic maps are known
from both sea turtles (Putman et al., 2011) and spiny
lobsters (Boles and Lohmann, 2003) and the Mexican
blind cave fish uses its lateral line organs to encode the
geometry and location of landmarks (Burt de Perera,
2004). In the latter study, the results suggested that the
cave fish develop cognitive maps based on exploration
of the environment without at any time being able to
perceive the whole environment at once. Spiders could
similarly rely on some simple form of a cognitive map
based on memories formed during spatial exploration of
the habitat.
There is currently no information available on how
such metric information could be gathered. Intriguingly,
however, the vertical descents discussed above could be
used to gather metric information on the size and shape
of the available free space in spiders that build vertically inclined webs. If the spider kept a more or less constant horizontal distance between each vertical descent,
it could estimate the available space in the horizontal
direction by counting the number of vertical descends it
can make without encountering obstacles. As discussed
previously, numerosity has been reported in jumping
spiders and might also be present in orb-web spiders
(Nelson and Jackson, 2012; Rodríguez et al., 2014).
Distances in the vertical direction could similarly be
estimated relatively easily by timing the vertical descents and using that as proxy for distance covered and
thus free space. Although perhaps more unlikely, spiders could also store the position of potential attachment
points encountered during site exploration in a manner
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similar to how landmarks are stored in social insects
(Cruse and Wehner, 2011; Shettleworth, 2010). During
the early phases of web-building spiders could then use
this stored information to guide their attachment of
anchor threads in order to ensure building a web as planar as possible.
4.2 The stigmergy hypothesis
Stigmergy, a type of emergent property or self-organised behaviour, is the expression of complex behaviour
based on interactions with, modifications of and feedback from the environment relying on simple rules. The
construction of circular walls built by grains around the
brood in a species of ants arises by stigmergy. Individual worker ants deposit grains based on the distance to
the brood and the local density of already placed grains
(Franks and Deneubourg, 1998). Similarly, spiders modify their environment by laying down silk threads which
again modifies the behaviour of the spiders encountering them (Krafft and Cookson, 2012). Social spiders
and spiderlings of solitary species appear to aggregate
in response to specific dragline attachment patterns and
silk densities (Saffre et al., 1999; Jeanson et al., 2004).
Orb-web spiders could thus rely purely on information
obtained from the silk threads that it trails behind during
site exploration (Zschokke, 1996), similar to how they
primarily rely on information gained from the distance
to the auxiliary spiral and to previously laid sticky spiral
threads for the exact placement of threads during construction of the sticky spiral (Hingston, 1920; Peters,
1970; Eberhard, 2012; Eberhard and Hesselberg, 2012).
A stigmergy model could in combination with cognitively simple binary information provide the spider with
all necessary information. Vertical descents could provide yes/no information on whether the space was obstacle free or not, while size suitability (suitable or not)
could be provided from the number or density of silk
threads (i.e. denser silk could mean the spider has
passed through the area many times during exploration
suggesting the site is small). Remote sensing using
chemical and vibrational stimuli could even provide
some metric information. The spider could for example
perhaps obtain length information by plucking a thread
similar to how it obtains information on the location and
size of prey trapped in its web by plucking radii
(Klärner and Barth, 1982; Foelix, 2011).
4.3 Predictions arising from the stigmergy and
cognitive map hypotheses
At present we do not have enough data to firmly reject or support either of the two hypotheses. However,
in Table 1 I have compiled some of the information and
HESSELBERG T: Exploration behaviour in orb-web spiders
predictions that in theory would allow us to distinguish
between them.
Exploratory webs: An exploratory web is a smaller
and less planar first web hypothesised to be built at a
new site (Zschokke and Vollrath, 2000). The spider then
slowly improves the quality of its web in subsequent
iterations. The presence of an exploratory web might
explain how spiders without relying on spatial memory
of the relative location of attachment points manage to
construct almost perfectly vertical and planar webs. In
contrast the cognitive map hypothesis postulates that
exploratory webs are not necessary as the spider has
gathered information on the location of suitable attachment points during exploration which it can rely on
during the early construction phases of the web. There
is some laboratory evidence that some spiders build a
smaller and less planar exploratory web on the first attempt to build a web at a new site (Zschokke and Vollrath, 2000; Nakata, 2004). However, studies on other
species of orb-web spiders found no evidence for an
exploratory web (Nakata, 2004; Hesselberg, 2013; 2014)
and the degree to which orb-web spiders in general rely
on exploratory webs under natural conditions remains
currently unknown.
Frequency of relocation after first web: If spiders do
not possess any information on the size of the available
space and instead rely on exploratory webs, we would
expect them to frequently have to relocate, when the site
where they build their smaller exploratory webs proves
not to be suitable for building the larger normal webs.
Unfortunately there is to my knowledge no available
observational or experimental data on the frequency of
relocations in the wild after construction of the first
web.
Abandoning site during exploration: The cognitive
map hypothesis predicts that spiders continuously gather information on the size and suitability of the site as
they explore it, while the stigmergy hypothesis predicts
that spiders first make an assessment after exploration
Table 1 Predictions of the cognitive map and the stigmergy hypotheses
Predictions/hypotheses
Cognitive map Stigmergy
Exploratory webs
Rare
Always
Frequency of relocation after first web
Rare
Often
Abandoning site during exploration
Often
Rarely
Complex proto-hub structure present
Rarely
Always
Removal of all threads leads to full
exploration
Rarely
Always
321
based on the number and density of threads laid down.
Both hypotheses though allow that site exploration can
be interrupted if obstacles in the free space are encountered. Nonetheless we would expect to see spiders leave
a site during exploration behaviour more often under the
cognitive map hypothesis than under the stigmergy hypothesis. Again I have not been able to find any data on
this.
Complex proto-hub always present: According to the
stigmergy hypothesis we would always expect a complex multi-stranded proto-hub to be present prior to
web-building as the silk threads contain the information
as to whether or not to construct the web as well as what
size and shape of web to construct. As mentioned in the
section above, the building of the web follows the construction of a proto-hub with either a simple Y-shaped
structure of three proto-radii or more commonly a proto-hub with up to 7 proto-radii (Peters, 1937; Eberhard,
1990b; Zschokke, 1996) and it is difficult to imagine
how such a simple structure in itself could provide adequate information on size and anchor point locations.
During site exploration the spider might attach threads
to particular good anchor points which end up being
incorporated into the proto-hub structure. However, this
would not work with a Y-structure since typical orb
webs in the field contain 4–10 anchor threads (7.3 ± 1.6
(mean ± std. dev., n = 130) based on rawdata of four
species from Hesselberg 2013). In contrast the cognitive
map hypothesis makes no predictions of the complexity
of the proto-hub. More quantitative information from
the wild on the proto-hub structure both during initial
web-building, but also during web-renewals is required.
Removals of all threads lead to full exploration: The
stigmergy hypothesis postulates that the the role of exploration behaviour is to leave silk threads behind
which will then be used subsequently to assess the quality of the site, while the primary aim of site exploration
according to the cognitive map hypothesis is to gather
and store spatial information. Thus if all silk threads
were removed following site exploration, the former
hypothesis requires a complete new exploration to be
carried out, while the latter hypothesis only require a
much shorter and more focussed renewal of key silk
threads to be rebuilt. Similarly if new spiders replace
original spiders after the latter have explored a site (i.e.
laid down trailing silk threads), but before they have
actually built a web, the stigmergy hypothesis predicts
that these new spiders could build a web without first
exploring it. This prediction could relatively easily be
tested in laboratory studies if spiders were replaced after
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Current Zoology
they had taken their old web down, but before they had
built a new one.
Although as mentioned above, we do not have
enough experimental evidence to reject any of the hypotheses, a number of studies suggest that spiders may
require some sort of spatial awareness and memory to
successfully build their webs. Firstly, while the simple
stigmergy hypothesis may be used by the spider for
determining if the space is suitable or not for a web, it
cannot easily explain (unless the silk threads or remote
sensing can provide some rough metric information) the
fact that many orb-web spiders manage to match the
shape of their webs to horizontal and vertical elongated
spaces (Fig. 2; Vollrath et al., 1997; Krink and Vollrath,
2000; Hesselberg, 2013). Secondly, as we saw in previous sections spiders adjust the size and shape of their
webs according to a host of environmental and previous
prey capture experiences (Heiling and Herberstein,
2000) and so probably have a target size and shape in
mind prior to initiating web-building, which they need
to ensure the available space can accommodate. This is
further supported by a study that found that spiders
match the size of their webs to their available silk reserves (Eberhard, 1988b). It is possible though that capture spiral size can be regulated independently of frame
size by constructing the web such that the area enclosed
by the frame is significantly larger than the area enclosed by the capture spiral (Eberhard, 1972). Nonetheless the spider would still need to ensure that there is
enough available space to build the minimum size of
frame structure allowing it to build its target sized web.
4.4 Suggestions for further experiments and results
of a preliminary study
As evident from the previous subsection, we first and
foremost require observational and experimental data to
test the predictions of the two hypotheses. However, in
addition we need more information on how site exploration is conducted by different spider species under
natural conditions in the wild. Most of our knowledge
comes from the spatially limited and structurally simple
conditions in the lab, but spiders in the wild may show a
very different behaviour. It is also likely that a proportion of the exploration performed by spiders in the lab
prior to web-building is done to look for ways in which
to escape the cage rather than to evaluate the site for
future web-building. While we have no way of knowing
when and where new webs will be constructed in the
field, one possible method would be to remove all silk
threads from existing webs on the site and release spiders caught from elsewhere onto it in the hope that they
Vol. 61 No. 2
will construct new webs there. Data could be obtained
by recording with one or more video cameras. In addition, in spiders that rest in retreats such as spiders in the
genus Zygiella and many tetragnathids, it might be
possible to modify the surrounding vegetation while the
spider is in its retreat and then record the ensuing exploration and web-building behaviour in order to assess
the importance of key attachment sites. Most of our
limited information on exploration behaviour comes
from spiders building vertical webs. It would be very
interesting to contrast and compare the behaviour of the
vertically building araneid spiders with spiders that
build more horizontal webs such as those in the genera
Gasteracantha (Araneidae), Leucauge (Tetragnathidae)
and Uloborus (Uloboridae), where for example vertical
descents such as those shown in Figure 3B would be
useless. However, in spiders that build vertical webs,
the possible role of the vertical descents is particular
intriguing. The first step to evaluate their importance is
to determine the degree to which they are performed
during construction of webs in the lab and in the field. If
the presence of vertical descents, as expected, is widely
confirmed, the second step would be to assess their role
in gathering metric and/or binary information from the
number of descents and descent duration as discussed
above. One way to do this would be to force spiders to
build webs in quadratic frames with long narrow vertical shaft extensions that prevent spiders from extending
their webs into them, but would increase the total drop
time and compare the size and shape of the resulting
webs with webs build in quadratic frames alone and
with webs build in quadratic frames with long narrow
horizontal shafts.
Another method would be to look at how spiders deal
with smaller obstacles in the available space to estimate
the potential spatial resolution of the exploration behaviour. A preliminary study doing just this with the
orb-web spider Argope argentata is shown in Fig. 4 (T.
Hesselberg, Unpublished data). Three cylindrical obstacles of different diameters were inserted (by tethering
them to wires) into the free space of the experimental
frames. The very preliminary results suggest that the
spiders adapt their web-building differently to large
obstacles (Fig. 4C) than to smaller obstacles (Fig. 4A,
B). Webs built in the presence of large obstacles were built
around the obstacle with the frame curving around it,
whereas webs built in the presence of smaller obstacles
showed no web-wide adaptation to the obstacles and
had the frame beyond the obstacle; in some cases even
completely enclosing it within the web (Fig. 4B). One
HESSELBERG T: Exploration behaviour in orb-web spiders
explanation for the observed web geometries in Fig. 4
could be that the spider noticed the large obstacle during
exploration and adapted its web accordingly prior to the
start of web-building, whereas the smaller obstacles
were first detected and responded to during radii and
spiral construction. This could again imply that some
kind of low-resolution spatial maps of obstacles were
formed during site exploration. However, much more
experimental work, including recordings of the actual
behaviour of the spiders prior to and during web-building, are required before any conclusions can be drawn.
It is also important to note that these experiments were
carried out in the lab where the spider had no option to
relocate. A different approach to estimate the information gathered during exploration would be to record the
behaviour and web geometry of webs built in situations
where the available space is reduced or enlarged in between the time the spider finishes exploration and starts
web-building. This could potentially be achieved by
getting spiders to build in frames with adjustable sides
although care would be required to ensure that any proto-radii maintained their tension. Finally, although as
highlighted above, more experimental work from both
the field and the laboratory is essential, computer simulations may also offer vital insights into the role of exploration behaviour. Computer models of the construction of the auxiliary spiral (Gotts and Vollrath, 1991) and
of the capture spiral (Eberhard, 1969; Krink and Vollrath, 1997; 1998) have previously shed light on the
rules governing these construction behaviours. Agentbased models, similarly to the one produced by Cruse
and Wehner (2011) to model the memory elements and
neural processing of navigation in desert ants in connection with the cognitive map hypothesis, might help
determine the level of information that spiders are required to collect during the exploration phase to successfully construct optimal orb webs at new sites.
Fig. 4
5
323
Conclusion
In this review we have seen how spiders despite a
relatively small and simple central nervous system show
a variety of complex cognitively demanding behaviours
including learning from previous prey capture, memory
of spiral turns, selective attention, potential numerosity
and an astounding behavioural flexibility allowing them
to adapt their webs to a wide range of internal and external factors. However, we have also seen how webbuilding itself although resulting in the highly structured and complex orb web may actually not be that
cognitively demanding and may instead rely on relatively simple rules of which many make use of previously constructed silk threads. The most cognitively
demanding task facing orb-web spiders may instead
relate to the initial assessment of new web-building sites.
However, too few studies have been conducted on exploration behaviour to date to draw any firm conclusions. Although it is probably unlikely that spiders possess cognitive maps as advanced as those whose existence is currently being hotly debated in social insects,
which are hypothesised to give bees and ants the ability
to infer and take novel short cuts between known locations (Gould, 1986; Menzel et al., 2005), it is equally
difficult to imagine how spiders would be able to build
well adapted orb webs at novel sites without relying on
some form of spatial memory involving basic metric
distances obtained during site exploration, especially
given their ability to match the size and shape of their
webs to confined spaces. One surprising outcome of this
review is that limited progress has been made in the
study of spatial cognition, exploration behaviour and the
early stages of web construction since Vollrath’s review
paper (Vollrath, 1992). This is particular remarkable
given the substantial progress achieved in our understanding of other aspects of web-building beha-
Webs built in experimental frames (30 × 30 × 5 cm) with obstacles by juvenile Argiope argentata
The photos show the first web built in a clean frame with an obstacle, so spiders are expected to have explored the frames prior to web-building. A.
A web built in a frame with a single small cylindrical obstacle (diameter of 2 mm). B. A web built in a frame with an intermediary obstacle (diameter of 7 mm). C. A web built in a frame with a large obstacle (diameter of 25 mm). The white horizontal scale bars represent a length of 5 cm.
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Current Zoology
viour and its flexibility and in our understanding of how
the web-building behaviour and the resulting web geometry interacts with the biomechanical properties of the
silk to create an optimal strong and light-weight aerial
trap (Vollrath and Selden, 2007; Harmer et al., 2011).
Recently there has been a renewed interest in the otherwise neglected area of spider neurophysiology with a
number of anatomical studies on brain size and structure
(Quesada et al., 2011; Park et al., 2013). Similar methods could be used to compare structures in the supraesophageal ganglion between spiders with extensive
site exploration to spiders with hardly any, such as the
Darwin’s bark spider (Gregoric et al., 2011), in order to
estimate the possible computational requirements of the
behaviour. Even more promising is the potential of
looking at the central nervous system of live spiders as
they perform behaviours with new and more sophisticated electrophysiological and neuroimaging techniques.
Finally technological progress may also soon provide us
with GPS tags of small enough size and a high enough
spatial resolution to directly track large orb-web spiders
such as species in the Nephila and Argiope genera during their site exploration behaviour in the wild.
I hope with this review to have provided some avenues for further research on the role of exploration behaviour in orb-web spiders and to have highlighted the
rich potential offered by these spiders and their webs for
enhancing our understanding of cognition, behavioural
flexibility and spatial learning in invertebrates.
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