A 30-year journey to fulfill a dream: social dominance networks reveal mechanisms promoting coexistence of charrs in streams of Hokkaido, Japan

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.

Plastic graph paper overlain on scale map of pools used to record data on the behavioral ecology of charrs (photo by K. Fausch).

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.

Shigeru Nakano, Satoshi Kitano, and Kurt Fausch (left to right) on the last day of the first summer of research in Poroshiri Stream, Hokkaido, July 1991 (photo from Fausch, 2018).

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.

Poroshiri Stream, Hokkaido, in August 2020, in the zone where Dolly Varden (top) and whitespotted charr (bottom) coexist (photos by S. Kitano).

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.


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.

Stressed-Out Squirrels

A recently-published paper in the Journal of Animal Ecology has discovered that the grey squirrel (one of the most impacting alien invasive species in Europe) causes an increase in chronic stress in the native red squirrel. Lead author Dr Francesca Santicchia is a research fellow at the University of Insubria in Italy. She had studied the relationships among parasites, physiological stress, and personality in grey squirrel / red squirrel interactions. In this blog post, she tells us more about her recent paper.

Our native red squirrels (Sciurus vulgaris) are threatened with extinction in large parts of the UK and Ireland and in areas in Northern Italy colonised by introduced invasive grey squirrels (Sciurus carolinensis). The replacement of native red by alien grey squirrels, a North America tree squirrel species, is a paradigm of the negative impacts induced by biological invasions on native ecosystems. It is based on two mechanisms of competition: food exploitation competition with grey squirrels strongly reducing the availability of tree seeds for red squirrels leading to a progressive reduction in the fitness of red squirrels; and disease-mediated competition where the grey squirrels acts as healthy reservoir for a shared pathogen, the squirrelpox virus, that causes high mortality in the native species.


Red squirrel (Photo: Ambrogio Molinari)

This was best of our knowledge on the red-grey squirrel paradigm before we demonstrated that invasive grey squirrels also cause an increase in chronic stress in native Eurasian red squirrels. In collaboration with teams from Austria and the US, we used a non-invasive technique to demonstrate that the occurrence of alien grey squirrels increases chronic stress of red squirrels living in the same forests.

grey squirrel_creditFrancescaSanticchia

Invasive grey squirrels compete for food with the native red squirrels, as well as transmitting the squirrelpox virus (Photo: Francesca Santicchia)

Mammals produce extra amounts of glucocorticoid hormones when trying to cope with harmful environmental stressors. However, when elevated glucocorticoid concentrations persist over longer periods of time, they often have negative effects on an animal’s fitness. Since these stress hormones are metabolized in the gut and excreted into the faeces, their concentration in faecal pellets – taken from red squirrels when they are captured for routine population dynamics studies – can be quantified as a stress parameter without the need of taking blood samples. When these concentrations of glucocorticoid metabolites excreted in faeces (FGM) are significantly higher than normal levels, they indicate an increase in chronic stress, a situation with potential devastating effects on the animal.

red squirrel_trapping_credit_FrancescaSanticchia

Faecal pellets were collected from captured red squirrels, allowing the team to measure the presence of stress hormones (Photo: Francesca Santicchia)

We predicted that since, for red squirrels, the ‘natural’ situation is being the only diurnal arboreal mammal in our woods, grey squirrels colonizing these habitats will act as a true environmental stressor. We tested this in three ways.

First, we compared FGM concentrations in individual red squirrels co-occurring with grey squirrels (red-grey sites), with FGM concentrations of squirrels in sites not colonised by the invasive species (red-only sites). Second, we monitored changes in FGM concentrations of red squirrels in two study sites that were colonised by the invader during our study (measuring FGM concentrations before and after colonisation). Thirdly, and finally, we removed grey squirrels in red-grey sites over a period of six months, and concomitantly monitoring changes in FGM concentrations in native red squirrels.

We found that native red squirrels in sites where they co-occurred with invasive grey squirrels had glucocorticoid concentrations that were three times higher than those in sites without the invasive species. Furthermore, in those woodlands colonised by grey squirrels, stress hormones in the local red squirrels increased after colonisation by the alien species. When we experimentally reduced the abundance of the invasive grey squirrels, the concentration of faecal glucocorticoid metabolites in co-occurring red squirrels decreased significantly between pre- and post-removal periods.

red squirrel handling_creditFrancesca Santicchia

Red squirrel populations could face extinction, partly due to increased physiological stress and food competition with greys (Photo: Francesca Santicchia)

This study shows that the invasive grey squirrel acts as a stressor which significantly increases physiological stress in the native red squirrel. This is a subtle form of interspecific competition, which may exacerbate the effects of food competition. In fact, both a lower food intake and chronic stress can produce a reduction in body growth and reduce reproduction among the red squirrels that are forced to share their habitat with the invaders. Ultimately, smaller size, lower fertility, and reduced recruitment of juvenile red squirrels will lead to the extinction of a population in few years’ time.

More info:

Santicchia et al. (2018) Stress in biological invasions: introduced invasive grey squirrels increase physiological stress in native Eurasian red squirrels. Journal of Animal Ecology, 87(5): 1342-1352.

Gurnell et al. (2004) Alien species and interspecific competition: effects of introduced eastern grey squirrels on red squirrel population dynamics. Journal of Animal Ecology, 73(1): 26-35.

How do birds avoid their sibling-species competitors?

Being similar can be problematic. When ecologically-similar species co-occur, competition can result. So how can this be avoided? A recent paper published in the Journal of Animal Ecology shows how birds avoid their sibling-species competitors. Authors Lechosław Kuczyński, Anna Skoracka, Jiri Reif and Radka Reifova explain.

Mechanisms that enable coexistence of ecologically-similar species are crucial in maintaining biological diversity. When such species co‑occur they inevitably compete for resources, such as space or food. This may lead to a local extinction of the inferior competitor or to segregation of species’ ecological niches.  This process is especially extreme in case of sibling species, which share both environment and traits due to their recent split from common ancestry.


Figure 1 The bird survey under way (Photo: Anna Skoracka)

Although the role of interspecific competition in niche differentiation has been the subject of intense studies, these mechanisms are still not fully understood. One of the reasons is the fact that the majority of studies have focused on ecological differences between species in areas of sympatry (where both species coexist within the same geographic area) against allopatry (when species’ ranges do not overlap). However, within a sympatric zone, there are sites which are occupied by both species (syntopic sites) or by only one of them (allotopic sites).  This pattern is often referred as a ‘mosaic distribution’.


Figure 2 The Common Nightingale (Photo: Cezary Korkosz)

Up to now, far too little attention has been paid to the problem how such mosaics arise and how competition contributes to niche segregation. Our research was aimed to fill this knowledge gap by including variation in co-occurrence within sympatry.  However to complete this task, a large-scale and long-term data spanning across allopatry and sympatry of the target species are essential. Gathering such data is beyond the capability of one research group realizing a single project within a restricted time framework. This is when a massive participation of volunteers and a broad social involvement come up to help to address a purely scientific question.


Figure 3 The Thrush Nightingale (Photo: Cezary Korkosz)

Biodiversity monitoring programmes undergo across the whole Europe since many years. They are based on data collected by skilled volunteers who use standardized protocols to gather relevant, scientifically rigorous, and broadly accessible information. The longest‑running and largest of these citizen science programmes are broad-scale bird monitoring projects (see European Bird Census Council web page for more information).


Figure 4 Breeding distribution of the Common Nightingale (orange) and the Thrush Nightingale (purple) in Europe. The study area (Poland) is highlighted by thick black line. Data for species’ geographic ranges were taken from BirdLife International (2017). (Image: Reif et al. 2018)

In our study, we have had an extraordinary opportunity to work with data collected within the Common Breeding Bird Survey in Poland, which runs since 2000 and involves engagement of almost a thousand of highly qualified volunteer ornithologists (Fig. 1). We used data on the abundance of two closely related bird species: the Common Nightingale (Luscinia megarhynchos, Fig. 2) and the Thrush Nightingale (Luscinia luscinia, Fig. 3) collected across their range involving both allopatry and sympatry.  These species diverged in the Early Pleistocene (approximately 1.8 Mya) and currently, co‑occur in a secondary contact zone spanning from Denmark through Germany, Poland, Ukraine, Hungary to the Black Sea (Fig. 4). Morphologically, they are almost identical. They differ in songs, nevertheless, heterospecific song copying occurs in sympatry. Occasional hybridization has been documented indicating that the reproductive barriers are not complete. Both species prefer the same dense shrubby habitats, mostly on moist sites, and their territories are often in close proximity.

Figure 5 all

Figure 5 The Common Nightingale escapes its sibling competitor by selecting drier, warmer and more elevated habitats often on the slopes of the hills (left). By contrast, the Thrush Nightingale moves towards wet lowlands, open pastures with willow bushes and colder climate in sympatry (right) (Photos: Radka Reifová)

We found that interspecific competition gave marked imprints on patterns in habitat preferences of these two nightingale species. Whereas the species preferred the same habitats in allopatry, their preferences became strikingly different in allotopy within sympatry where the abundance of the Common Nightingale increased towards dry and warm sites with low coverage of pastures (Fig. 5A), while the abundance of the Thrush Nightingale showed exactly opposite trends (Fig. 5B). It seems that both species “escape” from competition to allotopic sites covered by habitats avoided by the competitor (Fig. 6).


Figure 6 In allopatry, where both species are free from competition, they have similar habitat preferences. Within sympatry, their preferences diverge as a result of spatial segregation due to avoidance of the competitor. (Image: Reif et al. 2018)

Our findings are important because they show how biotic interactions may shape macroecological patterns. Moreover, they question the widely accepted view on the habitat preference as a species-specific trait invariant across its entire geographic range, as is often treated in analyses focused on modelling of species distributions. Instead, we found that species’ habitat preference is variable across space and depends on the context created by biotic interactions. This finding is particularly important nowadays, as species distribution models became a widely used tool for predicting the range shifts to adopt effective conservation strategies to mitigate climate change impacts. We argue that these models should incorporate biotic interactions, otherwise the model outputs will not provide meaningful guidance for conservation practice. Finally, our study emphasizes the value of data coming from monitoring programmes and the importance of dialogue between researchers and citizens, what is fundamental to biodiversity conservation.

More Info:

Reif, J., Reifova, R., Skoracka, A. and Kuczynski, L. (2018) Competition-driven niche segregation on a landscape scale: Evidence for escaping from syntopy toward allotopy in two coexisting sibling passerine species. Journal of Animal Ecology. DOI: 10.1111/1365-2656.12808