Vibrissal touch in the Etruscan shrew
The Etruscan shrew Suncus etruscus (also known as white-toothed pygmy shrew) is the smallest terrestrial mammal with a body weight of 2 g and a body length of around 4 cm without tail (Figure 1A). Shrews feed on insects and they use the sense of touch to detect and hunt prey. The elongated rostrum of the shrew has long whiskers referred to as macrovibrissae (Figure 1A, B); the shrew’s mouth is surrounded by a dense array of short whiskers, the so-called microvibrissae (Figure 1C).
Etruscan shrews belong to the family of Soricidae (shrews) and therein to the subfamily of Crocidurinae (white-toothed shrews)(Wilson and Reeder, 2005). It is widely believed that among recent mammals, shrews represent the closest relative to the ancestor of all placental mammals and the earliest shrew-like fossils date back approximately 70 to 100 million years ago (Archibald et al., 2001)
Etruscan shrews can be found from the Mediterranean to Southeast Asia in a belt extending between 10° and 30°N latitude (Figure 2). Their habitat includes scrub, open forest and grassland environments. In the Mediterranean region it prefers abandoned olive groves, vineyards, and other cultivated areas overrun by shrubs (Aulagnier et al., 2008). Being hunted by predatory birds and owls, shrews try to avoid moving uncovered in the open field, but rather seek shelter in old dry stone walls, under leaves or pieces of bark on the ground or in loose soil. They are specialized for a life in slits found in stone walls or piles of rock and they are able to enter and capture prey in slits as thin as 7 millimeters. Etruscan shrews successfully hunt and feed on insects that have almost the same body size as themselves and crickets are amongst their preferred food.
The small body size of Etruscan shrews goes along with an extraordinarily high energy turnover. They feed up to 25 times a day and consume more than their own body weight in food. Heart, respiratory system and skeletal muscles are functionally and structurally adapted to meet the enormous metabolic needs (Jürgens, 2002). In case of food restriction and at low ambient temperature, Etruscan shrews can reduce their body temperature and enter a resting state called “torpor” to cut down their energy expenditure (Fons et al., 1997). Traditionally, shrews (including Suncus etruscus) have been regarded as nocturnal animals. However, probably due to their constant food requirement, they may actually have a polyphasic circadian activity pattern with frequent activity bouts distributed over a period of 24 hours. This means that shrews have to be able to successfully hunt in twilight as well as in darkness, i.e., under conditions where vision is of limited use and, indeed, sight only seems to play a minor role. Work on relative shrew species from the Crocidura genus implicated vibrissae in navigation, but argued against the presence of echolocation in these animals (Grünwald, 1969).
A synopsis of sensory ecology of Etruscan shrews suggests the following picture: They live and hunt in slits inaccessible to larger animals. Here they rely on touch rather than on long-distance sensory modalities such as vision. Thus, shrews can be regarded as short-range/high-speed animals.
Tactile prey capture behavior
Etruscan shrew prey capture is guided by tactile cues (Anjum and Brecht, 2006). In a laboratory setting, hunting was filmed in total darkness under infrared illumination while crickets were offered as prey. These experiments demonstrated that Etruscan shrews attack in a precise and fast manner and that they need their whiskers to hunt successfully.
Spatio-temporal analysis of attacks on crickets
Spatial attack characteristics. Etruscan shrews place their attacks selectively on the cricket’s thorax (Figure 3 A, B) and manage to keep this precision regardless of the size of the prey. They attack crickets from the side with a narrow distribution of attack angles around 90° relative to the cricket’s body axis. Although most attacks are directed straight ahead, some shrews show a lateralization in their hunting: they preferentially attack with their head turned to their right rather than to their left side.
Temporal attack characteristics. Prey capture occurs very fast, in 80-200 ms per attack, with short inter-attack intervals of around 200 ms (Figure 3 C, D).
Attack dynamics. While first attacks are distributed relatively broadly over the cricket’s body, subsequent attacks are directed more and more precisely to the thorax with the help of corrective head turns that the shrews perform. Thus, shrews can use contact information from a distant body part of the cricket to guide attacks towards their preferred location.
Whisker dependence and tactile shape recognition
Both macro- and microvibrissae are required for hunting, with the macrovibrissae being particularly relevant for attack targeting. Shrews attack a plastic replica of a cricket but not other objects of similar size. Altering the shape of crickets by gluing on additional body parts from donor animals reveals that the jumping legs but not the head are key features in prey recognition. Addition of such “ectopic” jumping legs is highly confusing for shrews and leads to dramatic changes in attack pattern. The anterior thorax, a preferred target in normal crickets, is not attacked at all. However, the number of attacks targeted to the legs greatly increases. In summary, these experiments show that tactile shape cues are both necessary and sufficient for evoking attacks.
Shrews distinguish and memorize prey features and their prey representation is motion and size invariant. Shrew behavior appears to be based on the “Gestaltwahrnehmung” of crickets: they form a global construct of a cricket rather than only recognizing local elements. Thus, tactile object recognition in Etruscan shrews shares characteristics of human visual object recognition, but it proceeds faster and occurs in a 20,000-times-smaller brain.
Experience shapes tactile behavior in shrews
Little is known about the development of behavioral capacities in the somatosensory system. Three lines of evidence suggest that shrew tactile behaviors are not hard-wired but modified by tactile experience. The hunting behavior of young animals differs in subtle but significant ways from the hunting behavior of adults, whisker deprivation in young shrews disrupt the acquisition of normal hunting skills and shrews can acquire new hunting strategies in response to novel prey (Anjum and Brecht, in prep.)
The Etruscan shrew brain
Histological analyses as well as physiological techniques have been applied to assess the organization of the Etruscan shrew cortex. Based on Nissl and NeuN stains of coronal brain sections (Figure 4, left), the number of neurons is estimated to be ~1 million per cortical hemisphere, the surface area 11 mm² per hemisphere and the volume 4.5 mm³ (Naumann, 2008). The cortex is between 300µm to 600µm thick.
The small brain size of the Etruscan shrew and its thin cortex makes this animal uniquely accessible for imaging based approaches to study brain function. In particular, using two-photon-microscopy might allow visualizing the structure and function of cortical networks in unprecedented completeness (Figure 4, right; Roth-Alpermann, Houweling and Brecht, unpublished).
Cortical sensory areas have been delineated using multi-unit electrophysiological mapping of sensory responses (Brecht et al., submitted). Large parts of Etruscan shrew cortex (i.e. 60% of the total neocortical surface) respond to sensory stimuli. A small visual and a small auditory area have been identified. The majority of recording sites respond to tactile stimuli and more than half of these sites respond to macrovibrissae stimulation.
These findings demonstrate a remarkable degree of tactile specialization in the Etruscan shrew cortex. In comparison to other mammals studied so far, it is clear that the Etruscan shrew is one of the most extreme tactile specialists studied to date.
- Anjum, F., Turni, H., Mulder, P.G.H., van der Burg, J., Brecht, M. (2006). Tactile guidance of prey capture in Etruscan shrews. Proc Nat Acad Sci U S A 103(44): 16544-16549.
- Anjum, F. and Brecht, M. (in prep.) Tactile experience shapes prey-capture behavior in Etruscan shrews.
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