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Eight, the eye must have proper 4. Leys, S.P., and Degnan, B.M. (2001). The cytological basis of photoresponse behaviour phasing of the response. Je´ kely et al. in a sponge larva. Biol. Bull. 201, 323–338. [7] report at least an 80 ms delay to 5. Leys, S.P., and Meech, R.W. (2006). Physiology response, which must be compensated of coordination in sponges. Can. J. Zool. 84, 288–306. by an equal phase advance. Because 6. Arendt, D., Tessmar-Raible, K., Snyman, H., all rhodopsins respond to the change Dorresteijn, A.W., and Wittbrodt, J. (2004). Ciliary photoreceptors with a vertebrate-type in, rather than absolute, light intensity, opsin in an invertebrate brain. Science 306, the response occurs as the edge of 869–871. the field of view of the eye comes 7. Je´ kely, G., Colombelli, J., Hausen, H., Guy, K., Figure 2. Images of an animation at different Stelzer, E., Ne´ de´ lec, F., and Arendt, D. (2008). times of a helical path. into the light beam. The edge field is Mechanism of phototaxis in marine The helical path is described by its curvature, enhanced by the tubes of receptor zooplankton. Nature 456, 395–399. 8. Brown, D.A., and Berg, H.C. (1974). Temporal k, and the torsion with a k/t ratio of four being oriented perpendicular to the cell stimulation of chemotaxis in Escherichia coli. which is suitable for both organisms. The surface, which minimizes sensitivity Proc. Natl. Acad. Sci. USA 71, 1388–1392. Chlamydomonas eye (t negative, left handed) toward the normal and maximizes it 9. Tu, Y., Shimizu, T.S., and Berg, H.C. (2008). Modeling the chemotactic response of and the dorsal side of Platynereis larva toward a wide angle. Inadvertently, this (t positive, right handed) are facing inward. Escherichia coli to time-varying stimuli. Proc. optical trick may have made it easier to Natl. Acad. Sci. USA 105, 14855–14860. The normal vector, n, points directly toward 10. Foster, K.W., and Smyth, R.D. (1980). Light the helical axis. The direction of the helix, evolve polarization sensitivity since by antennas in phototactic algae. Microbiol. Rev. the net cell motion, is parallel to the Darboux shrinking the tube diameters 44, 572–630. vector [11], U(s) = t(s) t(s) + k(s) b(s), where s rhodopsins are forced into greater 11. Crenshaw, H.C. (1993). Orientation by helical is the length along the trajectory. Note this is motion. III. Microorganisms can orient to stimuli orientation along the long axis of by changing the direction of their rotational in the t–b plane. each tube as seen for many velocity. Bull. Math. Biol. 55, 231–255. 12. Crenshaw, H.C. (1996). A new look at invertebrate eyes [14]. Probably the locomotion in microorganisms: rotating and detect low light levels. Six, the spectral two eyes were also better to evolve translating. Am. Zool. 36, 608–618. sensitivity of the eye should match the stereovision. 13. Isogai, N., Kamiya, R., and Yoshimura, K. (2000). Dominance between the two flagella color of the incident light most useful The new paper by Je´ kely et al. [7] during phototactic turning in Chlamydomonas. for the behavior. The measured reminds us that there is a fascinating Zool. Sci. 17, 1261–1266. spectrum suggests an organism 14. Laughlin, S.B., Menzel, R., and Snyder, A.W. interplay between physical constraints (1975). Membranes, dichroism and receptor adapted to relatively deep waters. and evolutionary design for phototaxis, sensitivity. In Photoreceptor Optics, Seven, the eye must be integrated with which as a byproduct, via many A.W. Snyder and R. Menzel, eds. (New York: Springer-Verlag), pp. 237–259. the response mechanism of the cell for additional steps [15], led to eyes like 15. Lacalli, T. (2004). Light on ancient rapid communication of the signal. As our own. photoreceptors. Nature 432, 454–456. beautifully shown by Je´ kely et al. [7], 16. Foster, K.W., Josef, K., Saranak, J., and Tuck, N. (2006). Dynamics of a sensory signaling the photoreceptor cell acts as its own References network in a unicellular eukaryote. Conf. Proc. 1. Saranak, J., and Foster, K.W. (2005). The IEEE Eng. Med. Biol. Soc. 1, 252–255. motor neuron directly innervating via photoreceptor for curling behavior in Peranema cholinergic synapses and exclusively trichophorum and the evolution of eukaryotic inhibiting neighboring ciliated cells. rhodopsin. Euk. Cell 4, 1605–1612. Physics Department, Syracuse University, 2. Ehrenberg, D.G. (1838). Die Infusionsthierchen Syracuse, NY, USA. Although the synapse is probably by als vollkommene Organismen (Leipzig: E-mail: [email protected] chemical diffusion, the postsynaptic L. Voss), p. 547. 3. Saranak, J., and Foster, K.W. (1997). cells most likely respond electrically to Rhodopsin guides fungal phototaxis. Nature rapidly control the cilia. 387, 465–466. DOI: 10.1016/j.cub.2009.01.019

Tropical Ecology: Riparian Corridors this labor-intensive methodology has rarely been used in developing Connect Fragmented Forest countries [2,3]. Gillies and St. Clair [4] have broken new ground by Populations conducting the first direct experimental test of dispersal ability and corridor use in tropical forest . Landscape corridors connecting habitat patches may help overcome the The researchers removed barred genetic and demographic problems of small and isolated populations. An antshrikes ( doliatus) elegant field experiment shows that some Costa Rican forest birds will use and rufous-naped wrens ‘riparian’ (river margin) corridors to get back home, but they can be picky about (Campylorhynchus rufinucha) from corridor quality. their territories in Costa Rican dry forest and used radio tracking to map Cagan H. Sekercioglu biodiversity conservation [1]. To test their return paths [4]. After capture in the extent to which use a mistnet, a radio transmitter was Increasing human-domination and corridors between habitat fragments, attached to each bird (Figure 1), which fragmentation of tropical forests has one promising approach is to move was immediately translocated across made landscape and population them away from their territories and pasture, riparian forest or fencerows connectivity a critical issue for radio-track their efforts to return, but to a location 0.7–1.9 kilometers away. Dispatch R211

The birds could return back across pasture, along fencerows or through ‘riparian’ corridors (forested rivers). At riparian corridor translocations, antshrikes had 80% return rate, whereas this declined to 60% and 40%, respectively, for fencerow and pasture translocations. For wrens, there was no significant difference between treatments. At pasture and fencerow translocations, 80% of antshrikes used indirect forested routes to return, two crossed open pastures, and none used fencerows. However, only one out of 13 wrens, a species tolerant of open habitats, returned through forest, the rest traveling through fencerows or pastures in equal number. Both species crossed significantly fewer gaps while returning along riparian corridors than along fencerows or across pastures, but wrens crossed twice Figure 1. One of the barred antshrikes (Thamnophilus doliatus) in the study is about to be as many gaps as anthsrikes. radio-tracked after translocation. I spent a week with Gillies in July 2000 and these birds’ responses were apparent even then: barred antshrikes removed from their territories of its superfamily Furnarioidae, which mostly stuck to remnant forests, mainly individuals of ten Panamanian forest represents the main radiation of along riparian corridors, whereas land bird species with different forest-interior birds in the Neotropics rufous-naped wrens often made a run ecological requirements and forest [5]. Unlike the barred antshrike, 87% for it by flying across a pasture. What dependence. He released them over of Costa Rican furnarioid species struck me was the difference between Lake Gatun, Panama to measure how are forest-dependent [5], also Gillies’ Guanacaste location and my far they could cross a gap. The birds reflected in their sensitivity to forest Costa Rican field site near Panama. were highly motivated as the alternative fragmentation [7]. It would be Compared to Guanacaste’s open and was to drown (Moore saved them valuable to conduct a similar dry forest, the Las Cruces premontane when they fell in). Nevertheless, most experiment with species restricted forest is dense, humid, and gets four birds in forest-specialist families like to the tropical forest interior, as meters of rain per year. This is more could not cross even 100 these specialized species suffer representative of the less seasonal and meters of open water. Only 10% of most from the fragmentation and more diverse forests that comprise the Western Slaty-antshrikes, a forest isolation of their populations [2,8]. majority of tropical forests worldwide. interior species, could cross a 200 Landscape connectivity is critical in These humid forests harbor thousands meter gap. Over half of the birds tropical agricultural countryside where of bird, amphibian and other vertebrate could not cross 100 meters. Similarly, forest fragments harbor hundreds of species which, compared to these two in Brazilian Amazon, translocated species that rarely, if ever, leave the species, are more sedentary, more antbirds would not cross a 250 meter forest. In Guanacaste, where centuries forest-dependent, and more farm clearing to return to their of cattle raising practices have threatened. Their ability to use territories [2]. removed w75% of the native forest corridors is virtually unknown. Barred antshrike gives the classic that once covered the entire region [4], To put things into perspective, bird call of the Neotropics, a scolding most of the remaining forest outside Stiles [5] lists both study species as ha-ha-ha-ha-ha-ha-ha-ha-WAEYK that protected areas is found along forest-generalist/non-forest birds that is heard from to . fencerows and rivers. Nevertheless, are forest-independent. Of Costa Even though they are forest specialists 50–150 meter wide riparian corridors Rica’s approximately 700 land bird in Guanacaste, in the Neotropics, these and 15–30 meter wide fencerows of this species, Stiles [5] considered 60% birds are generally considered to be study are wider than many riparian more forest-dependent than barred forest independent [5], common in strips and fencerows seen in the antshrikes and rufous-naped wrens. forest edge and disturbed forest. A tropics, including my study area in That most of Gillies and St. Clair’s [4] widespread forest edge and thicket southern Costa Rica [9]. Considering birds returned to their original specialist rarely seen inside humid that both bird species tested are territories means they are reasonably forests, this species has adapted well forest-independent birds [5], more mobile for tropical forest birds. Many to the open, dry forests of Guanacaste. sensitive tropical forest species that forest-dependent species would not be Despite its reluctance to cross gaps often have access to narrower so lucky, even if their lives depended on in this study, the barred antshrike is corridors likely experience greater it. In a literal test of this, Moore [6] one of the more gap-tolerant species isolation and its consequences. Current Biology Vol 19 No 5 R212

Playback experiments in Chilean decline in isolated forest fragments that tropical countries, riparian temperate rainforest demonstrated lose their ‘service providers’ such as conservation laws are lacking, that corridors <10 meters were not seed dispersers [18] and insectivores insufficient or not enforced. We must used by forest understory birds and [7]. Therefore, higher landscape combine a better understanding of only corridors >25 meters were used connectivity, via corridors [18] or corridors with science-based constantly [10]. In Honduras, more increased tree cover in agricultural conservation and superior forest bird species and individuals areas [16] can have the added benefit enforcement to effectively conserve were recorded in belts 50 meters or of restoring some of these ecosystem these critical lifelines. Equally wider [11]. In Australian rainforest, services. importantly, local people need to be lemuroid ringtail possums require Corridors are likely to become more more involved with, informed about, corridor widths of at least 200 meters important as many species face range and benefit from corridor conservation [12]. In Amazonian tropical forest, shifts in response to climate change efforts in the tropics. corridors <200 meters wide are prone [19], but there is little knowledge on the to edge effects, and bird and mammal role of corridors in a changing climate References species richness declines in riparian [20]. Mobility does decrease the 1. Crooks, K.R., and Sanjayan, M.A. (2006). Connectivity Conservation (New York: corridors less than 400 meters wide chance of extinction in birds, as Cambridge University Press). [13]. These data hint that ideal tropical sedentary birds are 2.6 times more 2. Laurance, S.G.W., and Gomez, M.S. (2005). Clearing width and movements of forest corridor width may be inversely likely to be threatened or near- understory rainforest birds. Biotropica correlated with seasonality and directly threatened with extinction than long- 37, 149–152. correlated with regional species distance migrants [8]. By forcing many 3. Castellon, T.D., and Sieving, K.E. (2006). An experimental test of matrix permeability and richness. Wide corridors also serve as species to move to areas with suitable corridor use by an endemic understory bird. habitat in their own right and can harbor climate and vegetation, climate change Cons. Biol. 20, 135–145. 4. Gillies, C., and St. Clair, C.C. (2008). Riparian similar communities of litter frogs and will make mobility, connectivity, and corridors enhance movement of a forest small mammals as continuous corridors even more critical. Sedentary specialist bird in fragmented tropical forest. rainforest [14]. Two rows of trees do not birds, which include most bird species Proc. Natl. Acad. Sci. USA 105, 19774–19779. a corridor make, and in corridor [8], are five times more likely to go 5. Stiles, F.G. (1985). Conservation of forest birds ecology, width is as important as extinct from climate change than in Costa Rica: problems and perspectives. In Conservation of Tropical Forest Birds, length. long-distance migrants [19]. A.W. Diamond and T.E. Lovejoy, eds. The study birds, especially wrens, Riparian corridors also provide local (Cambridge: International Council for Bird regularly used stepping stones like ecosystem services by protecting Preservation), pp. 141–170. 6. Moore, R.P., Robinson, W.D., Lovette, I.J., and remnant trees to get back home [4]. watersheds for people and domestic Robinson, T.R. (2008). Experimental evidence Countryside biogeography [15] has animals, by reducing erosion, and by for extreme dispersal limitation in tropical forest birds. Ecol. Lett. 11, 960–968. shown that increased tree cover in providing shade and recreational 7. Sekercioglu, C.H., Ehrlich, P.R., Daily, G.C., tropical countryside not only improves areas [9]. Some tropical countries, like Aygen, D., Goehring, D., and Sandi, R. (2002). the mobility of forest-restricted Costa Rica and , have legislation Disappearance of insectivorous birds from tropical forest fragments. Proc. Natl. Acad. Sci. species, it also provides critical habitat that protects riparian corridors [13,14]. USA 99, 263–267. for many other forest species that Enforcement is a different matter, 8. Sekercioglu, C.H. (2007). Conservation ecology: area trumps mobility in fragment bird persist in these landscapes [9,15,16]. however, and riparian corridors are extinctions. Curr. Biol. 17, R283–R286. Since 2002, we have radio-tracked often much narrower and more 9. Sekercioglu, C.H., Loarie, S.R., Oviedo nearly 450 birds of ten native forest degraded than what is ideal for forest Brenes, F., Ehrlich, P.R., and Daily, G.C. (2007). Persistence of forest birds in the Costa Rican species persisting in the agricultural species [9,13]. Cattle also degrade agricultural countryside. Cons. Biol. 21, countryside of southern Costa Rica. riparian vegetation and make 482–494. 10. Sieving, K.E., Willson, M.F., and De Santo, T.L. Although riparian strips cover only corridors less suitable for native (2000). Defining corridor functions for endemic 4.6% of our study area, forest wildlife [9]. birds in fragmented south-temperate rainforest. generalist silver-throated tanagers As tropical landscapes become Cons. Biol. 14, 1120–1132. 11. Arcos, I.T., Jimenez, F., Harvey, C.A., and used them 23–38% of the time [9]. increasingly human-dominated, Casanoves, F. (2008). Richness and abundance Remnant trees, which provide deforested, and fragmented, riparian of birds in riparian forest belts of varied breadths at the Sesesmiles river stepping stones and fruits, were corridors are becoming microwatershed, Copan, Honduras. Revista used 31–48% of the time, despite disproportionably important in De Biologia Tropical 56, 355–369. covering 1.4% of the landscape. connecting and harboring populations 12. Laurance, S.G., and Laurance, W.F. (1999). Tropical wildlife corridors: use of linear Forest-dependent white-throated of tropical forest organisms. Gillies rainforest remnants by arboreal mammals. Biol. thrushes used riparian strips and St. Clair [4] have made an Cons. 91, 231–239. 13. Lees, A.C., and Peres, C.A. (2008). 29–35% and remnant trees 6–25% important contribution, but much Conservation value of remnant riparian forest of the time [9]. For some species, more is needed. Our knowledge of corridors of varying quality for Amazonian birds however, riparian habitat is not corridor use by tropical species is and mammals. Cons. Biol. 22, 439–449. 14. de Lima, M.G., and Gascon, C. (1999). The just an option. Worldwide, a quarter biased towards common species, conservation value of linear forest remnants in of tropical river specialist bird mobile endotherms, distributional central Amazonia. Biol. Cons. 91, 241–247. 15. Daily, G.C., Ehrlich, P.R., and Sanchez- species are near threatened, studies, and one time snapshots. We Azofeifa, G.A. (2001). Countryside threatened or extinct (my need more experimental studies in the biogeography: use of human-dominated unpublished data). tropics, focused on a wider range of habitats by the avifauna of southern Costa Rica. Ecolog. Appl. 11, 1–13. Birds themselves can connect taxa, representing threatened, 16. Tscharntke, T., Sekercioglu, C.H., Dietsch, T.V., landscapes with their ecological sedentary, and forest-dependent Sodhi, N.S., Hoehn, P., and Tylianakis, J.M. (2008). Landscape constraints on functional services such as pollination or nutrient organisms, while covering climatic diversity of birds and insects in tropical transfer [17]. These services can and elevational gradients. In most agroecosystems. Ecology 89, 944–951. Dispatch R213

17. Sekercioglu, C.H. (2006). Increasing awareness 19. Sekercioglu, C.H., Schneider, S.H., Fay, J.P., Center for Conservation Biology, Department of avian ecological function. Trends Ecol. Evol. and Loarie, S.R. (2008). Climate change, of Biological Sciences, Stanford University, 21, 464–471. elevational range shifts, and bird extinctions. 371 Serra Mall, Stanford, CA 94305, USA. 18. Levey, D.J., Bolker, B.M., Tewksbury, J.J., Cons. Biol. 22, 140–150. Sargent, S., and Haddad, N.M. (2005). Effects of 20. Haddad, N.M. (2008). Finding the corridor more E-mail: [email protected] landscape corridors on seed dispersal by birds. traveled. Proc. Natl. Acad. Sci. USA 105, Science 309, 146–148. 19569–19570. DOI: 10.1016/j.cub.2009.01.006

Visual Attention: The Thalamus at the attention in TRN was somewhat more modest than the increases in LGN but Centre? was nevertheless highly significant. This pattern of modulation was not observed prior to stimulus onset, New work shows that spatial attention modulates visual responses of single but only began in the initial neurons in monkey thalamus, providing empirical support for a long-standing 100 milliseconds after the stimuli theoretical prediction that specific thalamic nuclei play a key role in controlling appeared. Intriguingly, the modulation the spotlight of visual attention. was transient, disappearing in the next 100 millisecond epoch, but LGN cells Geraint Rees almost exclusively GABAergic also showed a second, later period of neurons. Both thalamocortical and modulation that could not be identified Until recently, visual attention and corticothalamic neurons emit in TRN cells. awareness in primates were thought excitatory collaterals within the TRN The receptive fields of LGN (and of as purely cortical phenomena. that are organised in both a spatiotopic TRN) cells are very small, and so But functional magnetic resonance and modality-specific fashion, and TRN detailed analyses of eye tracking data imaging (fMRI) signals in the human cells send strong inhibitory projections were able to rule out the possibility lateral geniculate nucleus (LGN) of to thalamic relay cells [4,5]. Thus, the that these findings could arise from the thalamus are correlated with inputs to the TRN are excitatory, but its systematic confounding by large or fluctuations in both visual attention and outputs to the same thalamic relay are small eye movements. Further visual awareness [1,2]. Such findings inhibitory (Figure 1). This suggests evidence that these effects derived are surprising, given the location of a possible modulatory role for the TRN from the top-down effect of spatial the thalamus very early in the visual in controlling thalamic activity, and led attention came from the observation processing pathway, and have sparked Francis Crick to suggest many years that these response modulations were a renewed interest in the functional ago [6] on theoretical grounds that the only seen on trials when the monkeys properties of the primate thalamus. TRN might play a key role in directing correctly detected the dimming of the Critical, but previously unresolved visual attention. peripheral target, and thus only on questions include whether such Nearly twenty-five years later, trials where spatial attention was modulation of fMRI signals reflect McAlonan et al. [3] recorded from correctly directed to the cued stimulus. changes in firing rate of individual LGN visually responsive neurons in the TRN Taken together, these findings show neurons rather than feedback signals and LGN of awake behaving macaque that attention leads to a spatially from cortical areas, and more generally monkeys performing a simple spatial specific biphasic modulation of what the precise functional relationship attention task. The monkeys fixated thalamic responses to visual stimuli: is between the different nuclei that on each trial, were centrally cued to an initial attenuation of TRN and comprise the primate thalamus. attend to one of two visual stimuli, and enhancement of LGN responses, McAlonan et al. [3] have provided then judged whether that stimulus followed by a slightly later important new data that not only subsequently dimmed. One of the enhancement restricted to LGN conclusively demonstrate that visual stimuli was placed in the receptive neurons. attention can modulate visual field of the recorded neuron and so These findings show that single responses of single cells in monkey the effects of attending to that stimulus neurons at very early anatomical stages LGN, but also provide significant new on visually evoked responses could of the visual pathway are already insights into the functional relationship be compared with when the same modulated by spatial attention. between different components of the stimulus was ignored. Attention Moreover, the comparison of LGN and visual thalamus. significantly increased visually evoked TRN modulation provides new insights The vast majority of visual responses in the LGN, and this increase into the functional relationship between information from the retina passes was independently observed in both different elements of local thalamic through thalamic relay cells in the magnocellular and parvocellular LGN circuitry. One intriguing possibility, lateral geniculate nucleus of the neurons. Critically, however, neurons in consistent with Crick’s [6] prediction, thalamus before reaching visual the TRN showed the opposite pattern is that the reciprocal early modulation cortex. Most axons connecting the of modulation: directing spatial of visual responses in both TRN and thalamus and cortex in either direction attention to a stimulus led instead to LGN reflects a causal influence of the pass through the thalamic reticular decreases in the firing rate of TRN TRN on the LGN. According to such nucleus (TRN), a thin shell surrounding neurons with receptive fields covering a proposal, the topographically the dorsal thalamus that contains that stimulus. This inhibitory effect of organised inhibitory collaterals from