This special issue is published on the occasion of the 100th anniversary of the Zeitschrift für vergleichende Physiologie (now “Journal of Comparative Physiology A”). It is also a clear statement of the importance of comparative research. I already had my first encounter with comparative biology as a student. In the animal physiology course, we had to prepare for each experiment. One of the textbooks that I used for my preparation was “Animal Physiology” from Heinz Penzlin. This textbook immediately captivated me because it was truly comparative. From Penzlin’s textbook I learned, for example, that the morphology and physiology of lungs, kidneys, brains and sensory organs can be very different in different animal species because different species live in different environments and thus are exposed to different selection pressures. My early enthusiasm for comparative biology finally led me to revise, together with Jan Hildebrand and Uwe Homberg, the “Penzlin” more than four decades later (Hildebrandt et al. 2020). As a student of biology, I also learned from the “Penzlin”—among others—that one can fully understand the morphology and physiology of an animal only if one considers its evolution and the natural environment in which this particular animal must function, i.e., if one does comparative research. No wonder that I submitted my first scientific manuscript to the “Zeitschrift für vergleichende Physiologie”. This journal, founded by Karl von Frisch and Alfred Kühn in 1924, was one of the few journals that at that time already emphasized the importance of the comparative aspects of physiological research. To my relief, my first manuscript was—after taking the suggestions of two reviewers into account—accepted for publication (Bleckmann 1980). This paper would be the first of 39 papers which I submitted and published in the Journal of Comparative Physiology A.

This article is not meant to be a review article of all my past work. Instead, I will summarize some of the various research projects we did in my laboratory but also how these projects came about. Since I recently have published an article about my lateral line research (Bleckmann 2023), this paper especially gives information about all the other research projects that I, together with my students, colleagues and collaborators have worked on. As the reader will learn, it was typically a combination of chance, curiosity and grant money that determined who I cooperated with and which animals’, respectively, scientific questions I investigated.

I wrote my diploma and doctoral thesis in the laboratory of Erich Schwartz from the University of Giessen. He and his students investigated the sensory basis of lateral line-mediated prey capture behavior in surface feeding fish (Schwartz 1965). With their cephalic lateral line, these fish detect and localize terrestrial insects trapped at the water surface. In the laboratory of Erich Schwartz, I already did my first comparative study. Among others, I found that both, the topminnow Aplocheilus lineatus and the butterflyfish Pantodon buchholzi, determine the distance to the center of a concentric surface wave by analyzing the frequency content, frequency modulation and curvature of the wave train. My studies were the first to show that two distantly related fish, although equipped with completely different cephalic lateral lines, do the same stimulus analysis for prey detection and prey localization. Furthermore, I uncovered that both species use all the hydrodynamic (physical) information theoretically available to determine the distance a surface wave stimulus has traveled (Bleckmann and Schwartz 1982; Hoin-Radkovski et al. 1984; Bleckmann 1988a).

In spring 1981, 1 year after my doctorate, Friedrich Barth from the University of Frankfurt offered me a postdoctoral position. The reason probably was that he was looking for someone who was familiar with the physics of water surface waves and had the motivation to study fishing spiders. Barth, who—for many years—served as the Editor in Chief for the Journal of Comparative Physiology A, already was an internationally recognized scientist who studied mechanosensation in spiders and spider behavior. He suggested that I should investigate the sensory basis of prey capture behavior in the fishing spider Dolomedes triton. Even though I would have to move from animals with backbones to invertebrates, I would stay with mechanoreception and the aquatic environment. This made my move from Gießen to Frankfurt easy.

Nearly all over the world, fishing spiders inhabit small ponds and the shoreline of lakes (Bleckmann and Rovner 1984). Like surface feeding fish, these spiders respond to capillary surface waves with a directed turn and a subsequent forward motion toward the wave source. One of the first things which struck me was the behavioral difference between surface feeding fish and fishing spiders, although both occupy the same ecological niche. Surface feeding fish tend to move around and show “emotions” (e.g., by rapidly oscillating their breast fins if frightened). In addition, these fish not only can learn, but also remember what they have learned over many weeks. Fishing spiders were different: for many hours, Dolomedes sat motionless at the edge of the experimental tank. While in ambush, up to four legs touched the water surface (Fig. 1). Since spiders cannot be conditioned, I relied on their innate behavior. I was somewhat frustrated that D. triton rarely responded to the wave stimuli I presented, but when it did so the response was usually very fast.

The fishing spider Dolomedes trition in lurking position at the edge of a pond

My research project in Frankfurt was part of a comparative study in which the sensory basis of prey detection in fishing spiders, web spiders and in spiders hunting on solid substrates was investigated by various laboratory members. I found that, unlike surface feeding fish, D. triton uses only the curvature of the wave front for distance determination (Bleckmann and Barth 1984). The large leg span of fishing spiders (about 4 cm) no doubt makes it easier for them to determine the curvature of a concentric wave stimulus. Many years later, my student Martin Borchard showed that the same holds true for the fishing spider D. okefinokensis (Bleckmann et al. 1994). I also found out how Dolomedes discriminates prey waves from non-prey waves, i.e., waves caused by wind, water drops or falling leaves. For this task, Dolomedes analyzes the frequency content, time structure and duration of a surface wave stimulus (Bleckmann 1985). Fishing spiders even weigh the amplitude–frequency content of a stimulus with respect to the distance the stimulus has traveled, taking the low pass filter properties of the water surface into account (Bleckmann 1988b). This shows that their stimulus-analyzing capabilities are as sophisticated as those of surface feeding fish. Thus, during my time in Frankfurt I learned for the first time that the small brains of invertebrates can perform as well as the much larger brains of vertebrates. In Barth’s laboratory, I was also involved in a study of the terrestrial wandering spider Cupiennius salei, a spider that is native to Central America and lives on banana plants and bromeliads. In a field study in Mexico, we measured the substrate-borne vibrations the spiders are typically exposed to when sitting on their dwelling plants. As Dolomedes, Cupiennius uses the frequency content, time structure and duration of a stimulus to discriminate prey from non-prey substrate vibrations (Barth et al. 1988a, 1988b). In retrospect, considering how orb-weaving spiders are adapted to read the vibrations of an insect trapped in a web (Klärner and Barth 1982), it is not surprising, given the diversity of spiders, that they would exploit this vibrotactile ability for any number of other prey capture scenarios.

Within the first 2 years after my PhD, Jochen Autrum, then Editor in Chief of the Journal of Comparative Physiology A, asked me to review a manuscript. I felt honored and consequently put a lot of effort into my review. Of course, the result was that I immediately received more manuscripts to review. Autrum did not mince words and very directly chastised me when the first manuscript I submitted to his journal was missing statistics. As a result, I got into the habit of always backing up my data with thorough statistics. One day, Autrum sent me the reports of the two referees on another manuscript I had submitted. In his accompanying letter, he wrote “There are two cases of stupidity. In the first case authors do not do the necessary statistics and in the second case they statistically back up data that are so clear that no statistic is needed.” I had to admit that Autrum was right.

In spring 1985, I moved to the Scripps Institution of Oceanography in San Diego (La Jolla, CA), to work in the laboratory of Theodor Holmes (Ted) Bullock, one of the most prominent comparative neurobiologists at the time. Although my spider studies had been very interesting I decided to return to the fish lateral line. One of my goals was to learn how to record from central lateral line units. Instead of working with teleost fish, we decided to work with cartilaginous fish. The reason was simple: Mechanosense in cartilaginous fishes was very much understudied compared with teleost fishes. At Scripps I recorded from central lateral line units of thornback guitarfish and hornsharks. I found that cartilaginous fishes process lateral line information at all levels of the neuraxis, from medulla to telencephalon. Like other studies (Schweitzer and Lowe 1984; Corwin 1991), my study showed that afferent pathways in the brain of elasmobranchs are much more like those in advanced vertebrates than was formerly believed (Bleckmann et al. 1987, 1989).

Soon after my arrival in La Jolla, I attended the International Conference on “Sensory Biology of Aquatic Animals” at the Mote Marine Laboratory in Sarasota, Florida. At this conference, organized by Art Popper, Dick Fay and others, I listened to a talk given by Uli Budelmann, a zoologist well known for his cephalopod studies. From Uli, I learned that cephalopods have lines of ciliated cells, called epidermal lines, on their head and arms. Without providing physiological evidence, Uli suggested that these lines function as hydrodynamic sensors (Budelmann 1988). Since Uli studied cuttlefish at the University of Texas in Galvaston, I invited him to come to the Scripps Institution of Oceanography to find out whether the epidermal lines of cephalopods are indeed sensitive to water motions. A few month later, when I picked him up from San Diego airport, he had 30 juvenile squids (Sepia officinalis and Lolliguncula brevis) in his hand baggage. Our initial attempts to get neuronal responses from the epidermal lines failed. But after we had tried out several electrode types, we succeeded in recording microphonic potentials and summed action potentials to single-frequency water motions. Similar to the fish lateral line (Bleckmann and Topp 1981; Bleckmann and Münz 1990; Münz 1989), minimal thresholds to local water displacements were found in the frequency range 75–100 Hz (Budelmann and Bleckmann 1988). The microphonic potentials recorded from the epidermal lines had twice the stimulus frequency, also in agreement with the microphonic potentials recorded from the fish lateral line (Flock 1965). Furthermore, responses were especially prominent at the onset of a stimulus. Our results proved that the epidermal lines of cephalopods are an invertebrate analog to the mechanoreceptive lateral line of fishes. In further experiments we found that the epidermal lines of cephalopods were extremely sensitive to abrupt frequency changes. A change of only 1 Hz, e.g., from 100 to 99 Hz, even at low stimulus amplitudes caused a clear neural response (Bleckmann et al. 1991b).

While in Ted Bullock’s laboratory, Glenn Northcutt was hired by the University of California San Diego. Before I met Glenn in San Diego, I was not especially interested in comparative neuroanatomy, but after several conversations with him, his postdoc Mario Wullimann and his PhD students Georg Striedter, Jaqueline Webb and Jiakun Song, I realized that comparative neuroanatomy is indeed another exciting branch of neurobiology. Now motivated to do some neuroanatomical studies, straight away and together with Eberhard Fiebig, a postdoc from Germany, I traced cell groups afferent to the telencephalon of Platyrhinoidis triseriata (Fiebig and Bleckmann 1989). Glenn and I also did a study on the pit organs of the axolotl Ambystoma mexicanum (Northcutt and Bleckmann 1993).

While in San Diego I was awarded a Heisenberg fellowship from the German Science Foundation (DFG) which would cover my expenses working in a laboratory of my choice. As it happened, a little later I received an invitation from Peter Görner from the University of Bielefeld (Germany) to work in his laboratory. After my arrival in Germany, I had to decide how to proceed scientifically. Because there were so many open questions still in lateral line research, I continued in this area. Until then, most researchers (including me) had stimulated the lateral line with mono-frequency water motions generated by a sphere that oscillated around a fixed position. That was a clean, but unfortunately very unnatural stimulus. Therefore I, Randy Zelick (Fig. 2) from Portland State University, and my PhD student Horst Müller, decided to stimulate the lateral line with the transient and irregular water motions generated by a small object that passed the fish laterally. Both, peripheral and central lateral line units, responded to such a stimulus. One exciting result was that some midbrain lateral line units were highly sensitive to the direction of object motion (Müller et al. 1996; Bleckmann and Zelick 1993). Since not much was known about the amplitude and frequency content of natural lateral line stimuli I measured, together with Thomas Breithaupt and Reinhard Blickhan, the water motions caused by rapid body or fin movements of fish, frogs and crustaceans. Furthermore, we characterized the water motions in the wake of a trout holding station in a flow tank. Our measurements revealed, that the recorded hydrodynamic events were mostly low frequency, but frequencies up to 100 Hz also occurred (Bleckmann et al. 1991a; Blickhan et al. 1992). Although low-frequency hydrodynamic events dominate in aquatic habitats (Kalmijn 1988), our experiments revealed that high-frequency water motions also occur under natural conditions. This made it clear why the fish lateral line not only responds to low-frequency, but also to high-frequency water motions.

Randy Zelick recording lateral line responses from the weakly electric fish Eigenmannia (around 1990). Reprinted with permission of Randy Zelick

Soon after my arrival in Bielefeld, I attended the Göttingen Neuroscience Meeting, organized by Norbert Elsner, his postdocs and students. While in Ted Bullock’s laboratory, I often had met Walter Heiligenberg (who unfortunately died in a passenger plane crash in1994). Walter and his students investigated the neural basis of the jamming avoidance response of weakly electric fish at the level of single cells. Since my encounter with Walter, I also had developed an interest in the electro sense. This was somewhat a natural extension of my research because, from an evolutionary perspective, the electrosensitive lateral line is a derivative of the mechanosensory lateral line. Strolling through the foyer of the conference building I met Gerhard von der Emde. Gerhard (who later became professor at the University of Bonn) presented a poster on the electric fish Gnathonemus petersii, and the work he was doing seemed to be very exciting. Like many weakly electric fish, G. petersii emits short electric pulses (electric organ discharges or EODs) day and night. Gnathonemus uses its self-emitted EODs for electro-communication, object identification and object localization (Moller and Bauer 1973). Depending on their electric properties, electrolocation objects alter the amplitude and wave form (phase) of an EOD. G. petersii senses its own EODs with specialized mormyromast electroreceptors distributed over most of the head and body surface. Inanimate objects (e.g,. stones) have purely Ohmic properties, whereas animate objects (e.g., other fishes, insect larvae or water plants) have a complex impedance consisting of a resistive (Ohmic) and a capacitive component. From behavioral experiments, Gerhard knew that G. petersii can discriminate purely Ohmic from capacitive objects. While Ohmic objects alter only the amplitude and not the wave form (phase) of the EOD, capacitive objects change both components of the locally perceived EOD. Mormyromast electroreceptors have two types of sensory cells, called A and B cells. Gerhard was convinced that either the A or the B cells must be phase sensitive and that Gnathonemus uses the response difference between A and B cells to discriminate between purely Ohmic and capacitive objects. Gerhard, who at that time was a postdoc in Bernd Kramer’s laboratory in Regensburg, had no access to an electrophysiological setup. Being interested in expending a bit into the domain of electroreception, I invited Gerhard to come work in my laboratory on the project (Fig. 3). A few months after the Göttingen meeting, he arrived in Bielefeld with 20 Gnathonemus petersii in his baggage. I was skeptical whether Gerhard’s hypothesis was right, but within 4 days we had evidence that only the B cells, but not A cells, responded to small phase shifts in the local EOD. Although the EODs of Gnathonemus have a duration of only 0.3 ms, a phase shift of just 1° was sufficient to alter the neural response (von der Emde and Bleckmann 1992). This was a nice example that showed that you can only ask the right question if you take into account the natural stimuli that a sensory system has to encode. Many researchers (including me) had recorded from primary mechanosensory lateral line afferents, but the responses of these afferents to a vibrating sphere stimulus were boringly similar in all species and fibers so far investigated (Münz 1989). No wonder that the clear response difference between A and B sensory cells was very exciting for me.

Gerhard von der Emde during our physiological experiments on the phase sensitivity of Gnathonemus in 1994. Reprinted with permission of Gerhard von der Emde

Much later, I presented our results to a general audience. After my talk, an elderly man came forward. He identified himself as a retired professor of physics. From him I learned that it is quite difficult for physicists to measure small phase differences. To learn more about the mechanisms used by Gnathonemus to detect minute phase shifts, he suggested a series of concrete experiments. We did these experiments (von der Emde and Bleckmann 1997), but unfortunately the experiments did not uncover the cellular mechanism of the extreme phase sensitivity of the B cells of Gnathonemus. Today, Gerhard thinks that it may not be the temporal phase shift to which the B cells respond. Instead, it could be the simultaneously triggered opposing amplitude shifts of the positive and negative phase of the local EOD evoked by a capacitive object that may cause the B cells to be more or less depolarized and thus to respond to even the smallest capacitive values (von der Emde et al. 2008; von der Emde and Zeymer 2020). As most biologists probably know, it is not easy to decipher the physical and molecular mechanisms that nature exploits.

In 1993, the University of Bonn offered me a full professorship. This allowed me, together with Joachim Mogdans and my new postdoc Michael Hofmann, to continue and extend my lateral line research. We were asking two main questions: first, what do natural lateral line stimuli look like? Up to now we had only studied the water motions caused by fish at a single point in the water column (Bleckmann et al. 1991a). To get information on the three-dimensional extension of fish wakes, my PhD student Wolf Hanke, in cooperation with Christoph Brücker (an engineer of fluid mechanics from the Technical University of Aachen, now professor at the City University of London) used the method of particle image velocimetry. We found that the wake behind a swimming goldfish shows a clear vortex structure for at least 30 s. Particle velocities significantly higher than background noise could still be detected 3 min after the fish (body length 10 cm) had passed (Hanke et al. 2000). This suggested to us that piscivorous fish (and other piscivorous animals equipped with hydrodynamic sensors) might be able to track fish wakes. We also found that the spatial dimensions of wakes caused by fish that differed in their style of locomotion were not all the same (Hanke et al. 2000; Hanke and Bleckmann 2004). Thus animals equipped with hydrodynamic sensors might not only be able to track fish wakes, but in addition may obtain some information about the originator of these wakes.

Our second question was: how does the peripheral and central lateral line cope with quasi natural lateral line stimuli? Since vortices and vortex streets are an important stimulus in natural waters (Rosen 1959; Blickhan et al. 1992) my PhD students Boris Chagnaud (now professor at the University of Graz) and Jan Winkelnkemper investigated how the peripheral and central lateral line responded to laminar water flow and to flow that contained vortices (Chagnaud et al. 2006, 2007; Winkelnkemper et al. 2018). In other studies, my PhD student Jacob Engelmann (now professor at the University Bielefeld) investigated how the fish lateral line separates signals from noise. Water motions were generated with a vibrating sphere or with an object that passed the fish laterally. Jacob found that the responses of primary afferents that received input from superficial neuromasts were masked in running water. In contrast, the responses of afferents that received input from canal neuromasts were not or only slightly masked (Engelmann et al. 2000, 2002a). This was the first study to show a biologically relevant clear difference in the responses of superficial neuromasts and canal neuromasts. Our study supported the idea that the lateral line of fish that have few superficial neuromasts, but a well-developed canal system is adapted to running water conditions, whereas the lateral line of fish that have only few superficial neuromasts is adapted to stillwater conditions (however, when we compared six stillwater with six running-water European cypriniform fish species, we did not find such a correlation (Beckmann et al. 2010)). In other studies, we investigated how central lateral line units cope with hydrodynamic noise (Engelmann and Bleckmann 2004; Engelmann et al. 2002b, 2003).

Pushing yet further, we investigated how space is represented in the central lateral line system (Voges and Bleckmann 2011; Meyer et al. 2012; Plachta et al. 2003). We not only compared stillwater fish with running-water fish, but also fish which had only few or many superficial neuromasts or which had an anatomical connection between the cephalic lateral line and the inner ear (Bleckmann et al. 1991c). Thus, our lateral line research was truly comparative and therefore entirely in the spirit of the Journal of Comparative Physiology A.

Nearly every year, I would attend the meeting of the German Zoological Society. In 1995, this meeting took place in Kaiserslautern. Walking through the poster exhibition hall, a poster that showed a forest fire caught my attention. One of the authors of the poster was Helmut Schmitz from the University of Erlangen. From Helmut, I learned that the pyrophilic beetle Melanophila acumilata (Buprestidae) approaches forest fires from large distances and that Melanophila most likely can detect the IR radiation emitted by forest fires with a pair of thoracic pit organs. Helmut went on to explain that the bottom of each pit consists of 50–100 sphere-like dome-shaped sensilla, each of which is innervated by the ciliary dendrite of a single nerve cell whose ultrastructure is similar to that of a ciliary insect mechanoreceptor. I knew the literature about infrared (IR) reception in snakes, but I had never heard of any insect capable of sensing IR radiation. According to Helmut, the pit organs of Melanophila most likely were sensitive to IR radiation, but physiological evidence was lacking. Since Helmut had no access to an electrophysiological setup, I invited him to come to my laboratory. Within 6 months, we were able to show that the pit organs of Melanophila are indeed sensitive to IR radiation, and this was the first physiological evidence of an insect IR receptor. The technique we used was similar to that I had applied to the lateral line neuromasts of the Axolotl Ambystoma mexicanum and the epidermal lines of cephalopods (Northcutt and Bleckmann 1993; Budelmann and Bleckmann 1988): the tip of a tungsten electrode was slightly advanced into a single dome-shaped sensillum of Melanophila. With this method, we learned that best sensitivity was in the wavelength range 2.8–3.5 μm, i.e., in a range that corresponded to the emission maximum of a forest fire. A stimulus intensity of 14.7 μW cm−2 was sufficient to generate a neural response. At higher intensities, a stimulus duration of only 2 ms reliably caused one action potential and in a repetitive stimulus regime receptor potentials showed characteristic fluctuations up to a stimulus frequency of 600 Hz. In crotalid snakes, the IR receptors work like a bolometer, where a thin membrane that is thermally isolated from the surrounding tissue is heated by IR radiation. Melanophila turned out to use a different mechanism. The pit organs of this beetle functioned according to a photomechanic principle: IR radiation causes the expansion of the cuticle of the IR-absorbing dome-shaped sensilla, which in turn squeezes the ciliary tip of the mechanosensory cell that innervates the sensilla. Such a photomechanic sensor was not shown before for any biological system (Schmitz and Bleckmann 1997, 1998; Schmitz et al. 1997, 2000a).

Helmut and I went on to study other insects capable of forest fire thermoreception. As with Melanophila, the Australian beetle Merimna atrata (Bupestridae) is attracted by forest fires (Fig. 4). And, again as with Melanophila, the larvae of this beetle obligatory depend on the wood of freshly burnt trees. We found (Schmitz et al. 2000b) that Merimna has two pairs of IR organs on the ventrolateral sides of its abdomen. However, these organs were fundamentally different from those of Melanophila. They consisted of specialized IR-absorbing areas, each of which was innervated by one thermosensitive multipolar neuron. If stimulated with IR radiation, the IR organs of Melanophila responded with a short latency in a phasic/tonic fashion. In contrast, the IR organs of Merimna compare best with the IR organs of crotalid and boid snakes (Amemiya et al. 1996): IR radiation is absorbed by a special surface and the resulting temperature increase in surface temperature is measured with a thermoreceptor. Most likely, Merimna used its IR organs to scan the surface temperatures of burned areas during low-level flight (Schmitz et al. 2000b, 2001). The Australian beetle Acanthocnemus nigricans (Acanthocnemidae) is yet another insect attracted by forest fires. Most likely, the larvae of this beetle depend on specialized Ascomycete fungi which become available after a forest fire. A. nigicans has a pair of IR organs on the first thoracic segment, each of which consists of a tiny sensory disc which absorbs IR radiation. To reduce heat conduction, each disc is arranged above an air-filled cavity. Inside each disc, about 90 multipolar thermoreceptors are tightly attached to the outside cuticle. Absorption of IR radiation leads to an increase of disc temperature which is sensed by thermoreceptors. The IR receptors of A. nigicans can also be best classified as microbolometers with reduced thermal mass (Schmitz et al. 2002). Such receptors resemble the IR receptors of pit vipers (Düring 1974).

Helmut Schmitz on a burned area in Australia looking for fire loving beetles in 2012. Inset: the pyrophilous beetle Merimna atrata. Reprinted with permission of Helmut Schmitz

Besides fire, warm-blooded animals are a natural source of IR radiation, albeit in a longer wavelength range. The haematophagous bug Rhodnius prolixus (Hemiptera) approaches mammals to get their blood (Schmitz et al.