Smell or vision? The use of different sensory modalities in predator discrimination

ABSTRACT Theory predicts that animals should adjust their escape responses to the perceived predation risk. The information animals obtain about potential predation risk may differ qualitatively depending on the sensory modality by which a cue is perceived. For instance, olfactory cues may reveal better information about the presence or absence of threats, whereas visual information can reliably transmit the position and potential attack distance of a predator. While this suggests a differential use of information perceived through the two sensory channels, the relative importance of visual vs. olfactory cues when distinguishing between different predation threats is still poorly understood. Therefore, we exposed individuals of the cooperatively breeding cichlid Neolamprologus pulcher to a standardized threat stimulus combined with either predator or non-predator cues presented either visually or chemically. We predicted that flight responses towards a threat stimulus are more pronounced if cues of dangerous rather than harmless heterospecifics are presented and that N. pulcher, being an aquatic species, relies more on olfaction when discriminating between dangerous and harmless heterospecifics. N. pulcher responded faster to the threat stimulus, reached a refuge faster and entered a refuge more likely when predator cues were perceived. Unexpectedly, the sensory modality used to perceive the cues did not affect the escape response or the duration of the recovery phase. This suggests that N. pulcher are able to discriminate heterospecific cues with similar acuity when using vision or olfaction. We discuss that this ability may be advantageous in aquatic environments where the visibility conditions strongly vary over time. SIGNIFICANCE STATEMENT The ability to rapidly discriminate between dangerous predators and harmless heterospecifics is crucial for the survival of prey animals. In seasonally fluctuating environment, sensory conditions may change over the year and may make the use of multiple sensory modalities for heterospecific discrimination highly beneficial. Here we compared the efficacy of visual and olfactory senses in the discrimination ability of the cooperatively breeding cichlid Neolamprologus pulcher. We presented individual fish with visual or olfactory cues of predators or harmless heterospecifics and recorded their flight response. When exposed to predator cues, individuals responded faster, reached a refuge faster and were more likely to enter the refuge. Unexpectedly, the olfactory and visual senses seemed to be equally efficient in this discrimination task, suggesting that seasonal variation of water conditions experienced by N. pulcher may necessitate the use of multiple sensory channels for the same task

Divergence of developmental trajectories is triggered interactively by early social and ecological experience in a cooperative breeder

Cooperative breeders feature the highest level of social complexity among vertebrates. Environmental constraints foster the evolution of this form of social organization, selecting for both well-developed social and ecological competences. Cooperative breeders pursue one of two alternative social trajectories: delaying reproduction to care for the offspring of dominant breeders or dispersing early to breed independently. It is yet unclear which ecological and social triggers determine the choice between these alternatives and whether diverging developmental trajectories exist in cooperative vertebrates predisposing them to dispersal or philopatry. Here we experimentally reared juveniles of cooperatively breeding cichlid fish by varying the social environment and simulated predation threat in a two-by-two factorial long-term experiment. First, we show that individuals develop specialized behavioral competences, originating already in the early postnatal phase. Second, these specializations predisposed individuals to pursue different developmental trajectories and either to disperse early or to extend philopatry in adulthood. Thus, our results contrast with the proposition that social specializations in early ontogeny should be restricted to eusocial species. Importantly, social and ecological triggers were both required for the generation of divergent life histories. Our results thus confirm recent predictions from theoretical models that organisms should combine relevant information from different environmental cues to develop integrated phenotypes

Leptobrachella brevicrus

<i>Leptobrachella brevicrus</i> <p>Colour in life and preservation (stage 25)</p> <p>The following description is based on five specimens at Stage 25 whose total length ranged from 16.50 to 46.50 mm (Tables 2 and 3).</p> <p>The skin of the head, body and tail is translucent brown. Dorsally (Fig. 2 C), the head and body are uniformly brown with small brown melanocytes. The colour of the snout is darker coffee brown, getting slightly lighter behind the ocular region. During ontogenesis the brown pigmentation changes from a light yellowish brown in smaller tadpoles to darker brown in larger specimens. In lateral view (Fig. 2 A), the brown pigmentation of the trunk changes from brown to an iridescent bluish-white colour. The spiracle is translucent and therefore difficult to distinguish from the body wall in lateral view. The lateral line system is clearly visible against the background colour. The nares have a beige interior surrounded by darker coffee brown pigmentation. The oral funnel is translucent. The eyes are black, with dark grey pupils in larger specimens. The pigmentation of the tail is light yellowish brown and the myotomes and myosepta are visible.</p> <p>Stage n BL BH BS BW ED ES IND IOD LFH MTH The dorsal and ventral fins are both unpigmented and opaque, pale yellowish brown. The tip of the tail is translucent. In ventral view (Fig. 2 B), the skin has a bluish–white sheen which is particularly intense between the oral disk and the hyobranchial apparatus. The skin of the dorsum and tail is translucent. In lateral and ventral views, the reddish gills, the pale yellowish liver and the gut coil are clearly visible through the skin.</p> <p> In preserved specimens (Fig. 2 F) the red colour of the gills and the brown pigmentation of head, body and tail disappear. The skin is transparent with a slightly darker bluish sheen. Myotomes and myosepta become more prominent. The oral funnel becomes translucent. The <i>vena caudalis ventralis</i> and <i>vena caudalis lateralis</i> are visible in ventral and lateral views. The eyes are uniformly black.</p> <p> <b>External morphological features.</b> The body shape is vermiform, the head and trunk are elongated and slender (Fig. 2 A). The trunk and head are subcylindrical. The head and belly are slightly depressed. The anterior tip of the head is rounded in lateral and dorsal views. The nares are closer to the snout than to the eyes (Fig. 2 C). The nares are round and open antero–laterally with a short dorsal projection. The internarial distance is subequal to the interorbital distance (Table 2). The eyes are positioned dorsolaterally. They are small and sunken and do not protrude beyond the body wall, the iris is uniformly black. The spiracle is sinistral, long and conical in shape and has a pointed end (Fig. 2 C). The spiracular tube protrudes from the body wall and opens laterally. The opening of the spiracle is positioned at 48–52% of the head–trunk length. The tail makes up 70% of the total body length. The dorsal fin is low in the proximal half of the tail, only broadening slightly in the posterior half. The height of the ventral fin is constant in the proximal half of the tail and only increases slightly in the posterior half. The upper and lower fin each contributes 25% to the maximum tail height. The tip of the tail is rounded. The muscles are visible through the transparent skin. The width of the base of the tail is 70–80% of the maximal trunk width. The anal siphon is short and dextral.</p> <p>The subterminal, antero-ventrally protruding oral disc can be seen from the both ventral and lateral aspects. The width of the funnel-shaped oral disc makes up 80% of the maximal width of the trunk (Fig. 2 A). The upper and lower lips each have deep medial emarginations (Fig. 2 E). The short and moderately pointed marginal papillae are arranged in a single row. Submarginal papillae are present on both sides between the oral orifice and the emarginations of the upper and lower lip and around the oral orifice. Below the submarginal papillae on the upper lip, two parallel parasagittal ridges emerge, run towards the upper jaw sheath and diverge laterally. On the lower lip a medial broad pad of thickened skin, parallel narrow ridges and isolated papillae are present. Keratodonts are absent. The beak is black and well keratinized with sharp serrations. The upper beak is arched in ventral view whereas the lower jaw is V-shaped.</p> <p>At Stage 39 the eyes protrude beyond the contour of the body. The oral disk and spiracle are reduced. All five toes are fully separated. Toe pads and subarticular tubercles are present. The tail is elongate and shows thick caudal muscles, the dorsal and ventral fins are not yet reduced.</p>Published as part of <i>Oberhummer, Evelyne, Barten, Catherin, Schweizer, Manuel, Das, Indraneil, Haas, Alexander & Hertwig, Stefan T., 2014, Description of the tadpoles of three rare species of megophryid frogs (Amphibia: Anura: Megophryidae) from Gunung Mulu, Sarawak, Malaysia, pp. 59-79 in Zootaxa 3835 (1)</i> on pages 66-69, DOI: 10.11646/zootaxa.3835.1.3, <a href="http://zenodo.org/record/286717">http://zenodo.org/record/286717</a&gt

Description of the tadpoles of three rare species of megophryid frogs (Amphibia: Anura: Megophryidae) from Gunung Mulu, Sarawak, Malaysia

Oberhummer, Evelyne, Barten, Catherin, Schweizer, Manuel, Das, Indraneil, Haas, Alexander, Hertwig, Stefan T. (2014): Description of the tadpoles of three rare species of megophryid frogs (Amphibia: Anura: Megophryidae) from Gunung Mulu, Sarawak, Malaysia. Zootaxa 3835 (1): 59-79, DOI: 10.11646/zootaxa.3835.1.

Leptolalax dringi

Leptolalax dringi Colour in life and preservation (stage 25) The following description is based on three specimens at Stage 25 with total lengths of 14.4 mm, 31.3 mm and about 56.5 mm (Table 2 and 3). In the larger specimen the distal part of the tail was removed for tissue sampling before preservation in formalin. The skin is a milky translucent ash grey. The skin of the head and trunk has an intense bluish-white sheen. Head and trunk are pigmented brown, the tail is darker coffee brown. On the dorsal face of the head and trunk, the muscular part of the tail and the dorsal and ventral tail fins, scattered irregularly shaped azure blue iridophores are present (Fig. 3 C), with those on the tail significantly larger. In lateral view (Fig. 3 A), the pigmentation of the trunk decreases from dorsal to ventral so that the ventral third of the lateral faces is unpigmented. Around the nares and orbits, unpigmented areas are present. Pigmentation in the smaller specimen is less developed, resulting in a lighter, more transparent appearance. The melanocytes of the muscular part of the tail are assembled to form V-shaped lines along the myosepta of the musculature. The dorsal and ventral fins (Fig. 3 A) are semitransparent and pigmented with melanocytes. Melanocytes are absent along the outer edges of the fins, with the unpigmented area broader on the ventral fin. In the smaller specimen the caudal fins are unpigmented. In ventral view (Fig. 3 B), the skin of the head, trunk and tail is unpigmented and translucent with a bluish-white sheen. The red gill tufts, heart, liver, and gut are visible through the skin. Forelimbs are not visible. The gut coil is visible in lateral and ventral views. After preservation the original brown pigmentation fades (Fig. 3 G), resulting in pale yellow colouration, the intense bluish-white sheen of the ventral face of the head and trunk disappears. The skin becomes more transparent. Most of the iridophores of the head, trunk, fins and tail are no longer visible. External morphological features. The body shape is oblong and depressed dorsoventrally (Fig. 3 A). The dorsal face of the head and body exhibits a longitudinal medial groove where left and right muscle blocks meet. The anterior tip of the head and the snout profile are rounded. The subterminal oral disc protrudes antero-ventrally and is only visible in lateral or ventral view. The nares are round and open anterolaterally. The rim of the nares bears a distinct mid–dorsal projection. The spiracle is sinistral. The cylindrical spiracular tube protrudes from the abdominal wall in its distal part only. The orifice of the spiracle opens postero–laterally and is positioned at 46–47 % of the head–trunk length. The tail makes up 73 % of the total body length. The eyes are sunken and do not project beyond the body wall, the iris is uniformly black. They are positioned dorsolaterally (Fig. 3 C) and are not visible in ventral view. The eyes are situated at 20–26 % of the distance between the anterior tip of the snout and the trunk–tail junction. The nares are oriented anterolaterally and are closer to the snout than to the eyes. The internarial distance is 66–107 % of the interorbital distance (Table 2 and 3). The dorsal and ventral fins rise slightly at the trunk–tail transition. The dorsal fin is flat/narrow in the proximal third of the tail. The edge of the dorsal fin is straight, while the ventral edge of the ventral fin is slightly convex. The muscular part of the tail makes up 46–54 % of the maximum tail height. The upper and lower fins both contribute around 25 % of the maximum tail height. The tip of the tail is rounded. The muscles are visible through the transparent skin of the tail. The width of the tail base is 69 % of the maximal trunk width. The anal siphon is dextral. The width of the cup-like oral disc makes up 44–50 % of the maximal width of the trunk. The oral disk is anteriorly and posteriorly emarginated along the medial plane. Marginal papillation (Fig. 3 D and E) is uniserial with a narrow anterior gap. Scattered submargical papillae are present posterior to the mouth. Papillae are short and rounded. The labial ridges bear uniserial rows of narrow, pointed and slightly curved keratodonts. In lateral view, there is a distinct hump on the distal third of the inner side of the keratodonts which separates the curved tip from the wider corpus. The size of the keratodonts decreases in the upper lip from anterior to posterior rows. In the lower lip their size decreases from posterior to anterior. The Labial Tooth Row Formula (LTRF) of the bigger specimen (Fig. 3 D) is 5 (2–5)/ 3 (1–2). In the upper lip keratodont row A- 1 is continuous and relatively narrow, four discontinuous rows follow caudally. Rows A- 2 and A- 3 have a medial divide, resulting in two lateral sections. Rows A- 4 and A- 5 are divided medially and again laterally, resulting in interrupted rows on both sides of the mouth. In the lower lip, rows P– 1 and P– 2 are divided medially, P– 3 is undivided. The Labial Tooth Row Formula of the smaller specimen (Fig. 3 E) is 4 (2–4)/ 3 (1–2). Rows A- 2 to A- 4 are only interrupted medially. The dark brown jaw sheaths are well–keratinized and robust. The upper beak lacks a medial notch and has small but sharp serrations. The serration of the lower beak is blunt. The upper jaw sheath is wide and arched. The lower jaw sheath is wide and V-shaped.Published as part of Oberhummer, Evelyne, Barten, Catherin, Schweizer, Manuel, Das, Indraneil, Haas, Alexander & Hertwig, Stefan T., 2014, Description of the tadpoles of three rare species of megophryid frogs (Amphibia: Anura: Megophryidae) from Gunung Mulu, Sarawak, Malaysia, pp. 59-79 in Zootaxa 3835 (1) on pages 69-71, DOI: 10.11646/zootaxa.3835.1.3, http://zenodo.org/record/28671

FIGURE 4. Megophrys dringi. A in Description of the tadpoles of three rare species of megophryid frogs (Amphibia: Anura: Megophryidae) from Gunung Mulu, Sarawak, Malaysia

FIGURE 4. Megophrys dringi. A) Tadpole at stage 25 in lateral view, golden pigment on the head, brown pigment on fin and in front of the eyes. B) Same individual in ventral view, only a small amount of pigmentation remains. C) Same individual in dorsal view, the tail is patterned golden/ brown. D) Adult individual. E) Overview of the oral disc of Megophrys dringi in preservation at Stage 25. Numerous submarginal papillae are found directly below the lips. F) Preserved tadpole at Stage 25 in lateral view showing typically faded pigmentation in contrast to living specimens. G) Drawing of tadpole at Stage 25 in lateral view

Data for divergance of develpmental trajectories.xlsx

Data for "Divergence of developmental trajectories" published in PNAS.<br

Animated images as a tool to study visual communication: a case study in a cooperatively breeding cichlid

Investigating the role of visual information in animal communication often involves the experimental presentation of live stimuli, mirrors, dummies, still images, video recordings or computer animations. In recent years computer animations have received increased attention, as this technology allows the presentation of moving stimuli that exhibit a fully standardized behaviour. However, whether simple animated 2D-still images of conspecific and heterospecific stimulus animals can elicit detailed behavioural responses in test animals is unclear thus far. In this study we validate a simple method to generate animated still images using PowerPoint presentations as an experimental tool. We studied context-specific behaviour directed towards conspecifics and heterospecifics, using the cooperatively breeding cichlid Neolamprologus pulcher as model species. N. pulcher did not only differentiate between images of conspecifics, predators and herbivorous fish, but they also showed adequate behavioural responses towards the respective stimulus images as well as towards stimulus individuals of different sizes. Our results indicate that even simple animated still images, which can be produced with minimal technical effort at very low costs, can be used to study detailed behavioural responses towards social and predatory challenges. Thus, this technique opens up intriguing possibilities to manipulate single or multiple visual features of the presented animals by simple digital image-editing and to study their relative importance to the observing fish. We hope to encourage further studies to use animated images as a powerful research tool in behavioural and evolutionary studies