Subtle physiological and morphological differences explain ecological success of sympatric congeners ANTHONY P. PORRECA,1,3, WILLIAM D. HINTZ,2 DAVID P. COULTER,1 AND JAMES E. GARVEY1 1
Department of Zoology, Center for Fisheries, Aquaculture, and Aquatic Sciences, Southern Illinois University, Carbondale, Illinois 62901 USA 2 Department of Biological Sciences, Darrin Fresh Water Institute, Rensselaer Polytechnic Institute, 110 8th Street, Troy, New York 12180 USA Citation: Porreca, A. P., W. D. Hintz, D. P. Coulter, and J. E. Garvey. 2017. Subtle physiological and morphological differences explain ecological success of sympatric congeners. Ecosphere 8(10):e01988. 10.1002/ecs2.1988
Abstract. Sympatric congeners with similar physiological and morphological characteristics may appear to overlap in niche space but respond to environmental change in different ways leading to population decline of one species while the other remains stable. Understanding why sympatric congeners vary in their ecological success can be challenging, but is particularly necessary given the magnitude of humaninduced environmental change among ecosystems. We propose that identifying a complex of subtle, interacting characters among congeners may be more effective in elucidating both historical coexistence and divergent ecological success in contemporary habitats compared to identifying just one apparent limiting similarity between species. Using this subtle difference hypothesis, we examined how metabolic rate associated with habitat use and internal and external morphology collectively influenced the ecological success of a common and a rare sturgeon species that differ dramatically in their conservation status due to environmental change. Multivariate analyses of gut morphology (e.g., intestine length) combined with respirometry on sand and gravel habitats were incorporated into a bioenergetics model to compare how the fishes responded to habitat change and food quality. Energetic tradeoffs induced by habitat type and underlying morphological differences led to different predicted growth rates. Compared with the more prevalent species, the rare and endangered fish needed to seek different habitats with less energetic costs and switch to foraging at a higher trophic level to persist. Our results corresponded to observed differences in ecological success between these species in the wild. Thus, subtle physiological and morphological differences may lead to dramatic differences in ecological success in contemporary habitats for species that are very similar ecologically. Key words: bioenergetics; endangered species; niche overlap; optimal digestion; rivers; species coexistence; sturgeon. Received 28 June 2017; revised 15 September 2017; accepted 26 September 2017. Corresponding Editor: Robert R. Parmenter. Copyright: © 2017 Porreca et al. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 3
Present address: Kaskaskia Biological Station, Illinois Natural History Survey, 1235 CR 1000N, Sullivan, Illinois 61951 USA.
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INTRODUCTION
1999) and proboscis lengths in bumblebees (Ranta and Lundberg 1980) allows for niche separation among these closely related competitors. However, niche differentiation between coexisting congeners may be subtle or not visually apparent (Siemers and Schnitzler 2004, Wellborn and Cothran 2007, Husemann et al. 2014), even when
Coexistence of similar congeners is often attributed to a single difference or limiting similarity (e.g., the size ratio of one morphological character; Hutchinson 1959). For example, the evolution of different beak sizes in Darwin’s finches (Grant
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similar congeners while remaining visually inconspicuous or subtle (Hilton et al. 2008, Griffen and Mosblack 2011). Metabolic tradeoffs are driven by both the food requirements of a consumer and energetic constraints imposed by the environment (e.g., through habitat use; Werner and Hall 1988, McPeek et al. 2001, Mittelbach 2002, Garvey and Whiles 2016). Foraging opportunities may permit the use of energetically unfavorable habitats (Werner et al. 1983, Biro et al. 2005). For example, Mueller and Diamond (2001) showed that species which evolve in environments where food resources are abundant are able to consume and assimilate energetic resources at a high rate and occupy different habitats than congeners that evolved in environments with less food. Both quantity and quality of food resources drive tradeoffs in digestive morphology between sympatric congeners (Sibly 1981). Species that consume small, hard-to-digest prey items (low-quality prey) typically have long intestines that increase surface area and retention time over which absorption of n and nutrients can occur (Sibly 1981, Carrasso Matallanas 1994), whereas species which consume large, high-quality prey often have shorter, simpler guts (Jobling 1995, Karasov and del Rio 2007). This broad pattern of morphology, identified by optimal digestion theory (Sibly 1981), is supported across a wide range of systems (Eubanks 2005, Stephens et al. 2007) and has been used to assess underlying differences between ecologically similar congeners. For example, gut morphology can effectively predict diet differences in congeneric Brachyuran crabs, allowing for comparisons between similar species that compete for food (Griffen and Mosblack 2011). Our objective was to examine if a complex of subtle characters can be used to explain differences in ecological success between ecologically similar sympatric congeners. We investigated whether a set of organismal features underlie niche differentiation as opposed to a combination of n-dimensional environmental conditions (Hutchinson 1957). We examined how oxygen consumption rate (a proxy for metabolic rate) associated with habitat use and internal and external morphology collectively may influence the ecological success of sympatric congeners that differ dramatically in their conservation status due to environmental degradation. Specifically, we tested if these organismal and environmental
one species experiences a significant decline while another exhibits positive or stable population growth. Differences between congeners may actually be closely adjusted to the ecological circumstances reflected in multiple morphological, physiological, or behavioral relationships between species (Wiens 1982). Thus, for coexisting congeners that have a different conservation status, identifying a complex of subtle characters in which species differ may be more effective in elucidating both historical coexistence and divergent ecological success in contemporary habitats compared to identifying just one limiting similarity between species (Hutchinson 1959). Currently, no study has explored how multiple subtle differences in morphology, physiology, and habitat use collectively influence ecological success between similar congeners. Ecological success is a measure of a species’ ability to persist through time and is driven by multiple factors that cause differential survival and reproduction (Wilson 1987). Thus, the status and abundance (i.e., population trends) of congeners can be thought of as measures of ecological success between species, where species with stable or increasing populations are more successful than species experiencing decline. In general, there is a poor understanding of why some species are threatened with extinction and their congeners are not (Beissinger 2000), which may be because the scale at which subtle differences exist between species is not captured by traditional species monitoring (Hintz et al. 2016a). Detailed information on the ecology of rare congeners may also be limited by data only collected from environments modified by humans (Western 2001), where anthropogenic disturbances can affect sympatric congeners in similar or different ways. For example, differential responses by similar congeners may be more common in conjunction with anthropogenic disturbance, such as habitat loss or harvest, because these threat processes are often specific to species’ underlying differences in biology (Owens and Bennett 2000, Isaac and Cowlishaw 2004). However, it is unknown how evolved complexes of subtle characters that promoted niche differentiation between species may lead to different responses to environmental change. Metabolism and digestive morphology are two traits that can influence ecological success among ❖ www.esajournals.org
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difference hypothesis may explain major differences in the conservation status of ecologically similar sympatric species.
factors aligned with the current status of the very rare and endangered pallid sturgeon (Scaphirhynchus albus) and a more abundant sympatric congener, the shovelnose sturgeon (Scaphirhynchus platorynchus). Worldwide, sturgeons are the most at-risk group of fishes and all sturgeon species inhabit large rivers, which are among the most modified freshwater ecosystems (Pikitch €ro €smarty et al. 2010). As young, et al. 2006, Vo pallid and shovelnose sturgeon overlap in habitat use, diet, and are morphologically similar (Sechler et al. 2013, Hintz et al. 2016b; Fig. 1), but adult pallid sturgeon are piscivores and adult shovelnose sturgeon remain invertivores. Despite significant ecological similarity between species, little or no successful recruitment of pallid sturgeon has been observed in decades (Boley and Heist 2011), while shovelnose sturgeon have remained stable (Phelps et al. 2016). We hypothesized that although they appear similar, pallid and shovelnose sturgeon would exhibit subtle differences in morphology and physiology during early life, which account for their conservation status later in life. We suggest a subtle
METHODS Animal husbandry We acquired genetically pure pallid sturgeon and shovelnose sturgeon as larvae from Gavins Point National Fish Hatchery (Yankton, South Dakota, USA) and the United States Geological Survey’s Environmental Research Center (Columbia, Missouri, USA), respectively. Larvae were first generation spawn from wild-caught broodstock. Upon acquisition, larvae were acclimated to a recirculating aquaculture system equipped with filtration to remove particulates and biofiltration to transform toxic metabolites. Both shovelnose and pallid sturgeon were raised in the same recirculating system and thus similar environmental conditions (e.g., temperature, dissolved oxygen, water quality, and flow conditions were identical) but kept in separate tanks to maintain species identity. Salinity was maintained at 1 ppt,
Fig. 1. Left: Age-0 pallid sturgeon (left) and shovelnose sturgeon (right) at approximately 6 months old. These species appear to be nearly morphologically identical at this life stage. Right: External and internal structures associated with food acquisition and digestion in Scaphirhynchus sturgeon. Internal anatomy redrawn from Weisel (1979).
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ammonia
