This blog post is provided by Kurt D. Fausch, Satoshi Kitano, Yoichiro Kanno, and Seog Kim and tells the #StoryBehindThePaper for the article “Interspecific social dominance networks reveal mechanisms promoting coexistence in sympatric charrs in Hokkaido, Japan”.

Some papers take a long time to come to fruition…. sometimes a very long time. Kurt Fausch first traveled to Japan in October 1988, to present an invited paper at an international symposium on charrs in Sapporo, Hokkaido. There he met a young fish biologist, Shigeru Nakano, who had collected large amounts of very detailed data on the behavior of charr and landlocked masu salmon in several streams across Japan. For example, during three studies he recorded from 856 to 2835 aggressive encounters among individuals arranged in dominance hierarchies in pools, and in one study he snorkeled for an amazing 41 consecutive days (Fausch 2018). Fausch encouraged him to publish his work in international journals, and decided that he needed to collaborate with this amazing young scientist.

That encounter led to a collaboration that lasted more than a decade. Fausch was keenly interested in how native stream salmonids coexisted along riverscapes, and how nonnative salmonids excluded native ones. At the symposium, Nakano introduced Fausch to Dr. Kenkichi Ishigaki, and his book Exploring the Mystery of Charrs (Ishigaki 1984) detailing his research on the zoogeography, ecology, and behavior of Dolly Varden and whitespotted charr, closely-related congeners that inhabit Hokkaido streams. The patterns were so intriguing that Fausch asked Dr. Hiroya Kawanabe, the symposium organizer and elder statesman of ecology in Japan, how to collaborate with Nakano. Together, they crafted a proposal to a joint U.S.-Japan program, and after the INTECOL meetings in Yokohama in 1990, Nakano took Fausch and two Japanese graduate students deep into the mountains of Hokkaido, to introduce them to the Poroshiri catchment where both charr coexisted (see Fausch, 2015).

In their subsequent research with Ph.D. student Satoshi Kitano during 1991-1994, they sought to understand everything they could about these two species, from zoogeographic patterns across Hokkaido Island, to their distributions along catchments, and how they interacted in dominance hierarchies in individual pools. Fausch and Nakano believed that to understand the mechanisms that allowed these charr to coexist, they needed to understand their zoogeography, evolution, ecology, and behavior as thoroughly as possible, and across spatial scales. Following on Ishigaki’s pioneering work, these studies confirmed that the distribution of the two species was closely related to temperature, with Dolly Varden in the colder headwaters and whitespotted charr downstream. The zones where they coexisted across catchments coincided with a consistent air temperature isotherm, and an approximate mean summer water temperature of 7-9 ^oC.  Moreover, this temperature zone shifted across the island, from the cold northeast peninsula in the North Pacific Ocean to the warmer southwestern tip bordered by the Sea of Japan.

But Shigeru Nakano’s real gift was his ability to make detailed observations of the positions, foraging, and agonistic interactions among charr in the step pools of steep mountain streams like Poroshiri, a skill he had developed during his previous studies, and his Master’s research on cichlids in Lake Tanganyika (Fausch 2018). He taught Fausch how to map pools and record the behavioral data on plastic graph paper overlays. In turn, Fausch taught Nakano how to design controlled experiments in the field. Moreover, Nakano and Furukawa-Tanaka (1994) had previously found that Dolly Varden could shift their behavior from normal sit-and-wait foraging on drifting invertebrates to ranging throughout pools and picking benthic invertebrates from the substrate, a behavior that proved important for species coexistence.

Nakano and Fausch made intensive 5-week field expeditions to Poroshiri Stream during summer 1991 and 1992, and Nakano continued research for two more years, resulting in papers about charr distributions (Fausch et al. 1994) and experimental and observational studies showing that the foraging shift was caused by seasonal declines in drifting invertebrates (Fausch et al. 1997; Nakano et al. 1999). But the manipulative experiment Fausch planned to test the relative strength of interspecific versus intraspecific competition between the two charr failed, a major disappointment. Fish movement destroyed carefully manipulated densities in pools, and fences were not feasible in the high-energy stream. Instead, Nakano suggested that they simply record the foraging and agonistic behavior of charr in their interspecific dominance hierarchies.  Fausch proposed that they successively remove the most dominant fish to “titrate” the hierarchies, and determine the positions for which fish competed. Nakano was skilled at using Japanese traditional keiryu angling with live invertebrates, while observing the fish underwater by snorkeling, an excellent method to capture the most dominant charr with little disturbance to the rest. Nakano, Kitano, and Fausch spent many hours snorkeling in cold water to collect the data, long before the invention of Go-Pro waterproof cameras.

It seemed to Fausch that because stream salmonids compete for foraging positions in hierarchies based on size that the pattern of dominance between the two species could reveal the relative strength of competition. For example, if interspecific competition by one species was stronger than intraspecific competition, then smaller individuals of that dominant species should dominate larger individuals of the subordinate species. In contrast, if interspecific and intraspecific competition were equal, then size alone would determine dominance, not species. As often happens, while he pondered whether this theoretical framework held merit, other life responsibilities intervened and the analysis languished. Finally, when he retired, there was time to take up the ideas again.

This work took on renewed importance to Fausch because after their decade of collaboration Shigeru Nakano had been lost in a tragic accident in the Sea of Cortez in March 2000 (Fausch, 2000). Fausch and his colleagues spent much of the next decade following up on Nakano’s research legacy in stream-riparian food webs, publishing papers on that topic, creating a documentary film about his life (RiverWebs), and writing a book that included many research experiences in Japan (Fausch, 2015). In addition, they recently published another study Nakano led, showing that Dolly Varden jaw morphology shifted when together with whitespotted charr, allowing the Dolly Varden to forage more on benthic insects than when alone and providing evidence for character displacement (Nakano et al., 2020).

However, good things come to those who wait. In discussing the data on dominance hierarchies with Dr. Yoichiro Kanno and his graduate student Seog Kim, Fausch found that their knowledge of exponential random graph models in the rapidly-developing field of social network analysis could be applied to this problem. Likewise, the successive removals Fausch and Nakano conducted are now labeled “knockout experiments” and considered a powerful direct method to determine dominance (Pinter-Wollman et al., 2014). In addition, new papers highlighted the importance of testing the mechanisms underlying species coexistence (McPeek & Siepielski, 2019). Despite the apparent failure to carry out a daunting manipulative field experiment, when the data were analyzed after nearly 30 years everything fell into place.

The upshot is that water temperature provides an equalizing mechanism that controls distribution of the two species along Hokkaido streams. In relatively narrow zones of sympatry defined by temperature, whitespotted charr do not dominate and exclude Dolly Varden, resulting in similar fitness for the two species. This study (Fausch et al., 2020) shows that in individual pools in this zone, the two species treat each other as equals and dominance is based on size alone. However, as drifting invertebrates decline throughout summer, Dolly Varden shift to foraging on bottom-dwelling invertebrates, facilitated by the shift in jaw morphology which apparently increases their foraging efficiency (Nakano et al., 2020). These shifts allow the two species to partition food resources, and provide a modest stabilizing mechanism that balances the remaining differences in fitness. As further evidence for their coexistence, when Kitano returned to Poroshiri Stream in August 2020, a snorkeling survey of the entire segment showed that the two charrs had identical distributions, even after 30 years.

The theoretical framework developed here for analyzing data on interspecific dominance hierarchies (Fausch et al., 2020), coupled with additional studies on tradeoffs in ecological performance based on temperature and foraging and morphological shifts, provide a body of evidence that helps explain why and how these two charrs coexist across Hokkaido catchments.  The result fulfills the dream that Shigeru Nakano and Kurt Fausch had when they began their collaboration in 1990 to further explore the mystery of charrs. Somewhere, Nakano-san must be smiling.

References

Fausch, K. D.  (2000).  Shigeru Nakano: an uncommon Japanese fish ecologist. Environmental Biology of Fishes, 59, 359–364.

Fausch, K. D.  (2015).  For the love of rivers: a scientist’s journey.  Corvallis, OR: Oregon State University Press.

Fausch, K. D.  (2018).  Crossing  boundaries: Shigeru Nakano’s enduring legacy for ecology.  Ecological Research, 33, 119–133.

Fausch, K. D., Nakano, S., & Ishigaki, K.  (1994). Distribution of two congeneric charrs in streams of Hokkaido Island, Japan: considering multiple factors across scales. Oecologia, 100, 1–12.

Fausch, K. D., Nakano, S., & Kitano, S.  (1997). Experimentally induced foraging mode shift by sympatric charrs in a Japanese mountain stream.  Behavioral Ecology, 8, 414–420. 

Ishigaki, K.  (1984).  Exploring the mystery of charrs (in Japanese).  Tokyo, Japan: Iwanami-shoten,

McPeek, M. A., & Siepielski, A. M.  (2019).  Disentangling ecologically equivalent from neutral species: The mechanisms of population regulation matter.  Journal of Animal Ecology, 88, 1755-1765. 

Nakano, S., & Furukawa-Tanaka, T.  (1994).  Intra- and interspecific dominance hierarchies and variation in foraging tactics of two species of stream-dwelling chars.  Ecological Research, 9, 9–20.

Nakano, S,, Fausch, K. D., & Kitano, S.  (1999).  Flexible niche partitioning via a foraging mode shift: a proposed mechanism for coexistence in stream-dwelling charrs.  Journal of Animal Ecology, 68, 1079–1092. 

Nakano, S., Fausch, K. D., Koizumi, I., Kanno, Y., Taniguchi, Y., Kitano, S., & Miyake, Y.  (2020).  Evaluating a pattern of ecological character displacement: charr jaw morphology and diet diverge in sympatry vs. allopatry across catchments in Hokkaido, Japan.  Biological Journal of the Linnean Society, 129, 356-378. 

Pinter-Wollman, N., Hobson, E. A., Smith, J. E., Edelman, A. J., Shizuka, D., de Silva, S., … McDonald, D. B. (2014). The dynamics of animal social networks: analytical, conceptual, and theoretical advances.  Behavioral Ecology, 25, 242-255.