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Investigating fishing strategies and habitat differences in late Holocene Oregon Coast sturgeon (Acipenser spp.) through coupled genetic and isotope analyses

Authors:

Abstract

Understanding the habitats people were fishing in the past is central to evaluating the relationship between coastal environmental change and human behavior. Researchers often use zooarchaeological identification of fishes and modern ecological data to infer the habitats people fished in the past. However, these inferences assume stable environmental conditions through time and can be hindered by precision issues in identification of archaeological specimens (species vs. genus or family). Here, we integrate genetic and bulk tissue stable isotope data to investigate a late Holocene sturgeon fishery in northern Oregon. Ancient DNA analysis indicated that people were fishing for both green and white sturgeon (Acipenser medirostris and Acipenser transmontanus) in comparable numbers. Stable isotope analyses of these same bones documented distinct isotope values for each species, correlating with species-specific habitat preferences. These findings highlight the value of paired isotope and genetic data to elucidate human fishing strategies and environmental change and provide baseline ecological data for modern fisheries.
Quaternary Science Advances 7 (2022) 100062
Available online 19 September 2022
2666-0334/© 2022 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Short Communication
Investigating shing strategies and habitat differences in late Holocene
Oregon Coast sturgeon (Acipenser spp.) through coupled genetic and
isotope analyses
Emma A. Elliott Smith
a
,
*
, Torben C. Rick
a
, Courtney A. Hofman
b
,
c
a
Department of Anthropology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA
b
Department of Anthropology, University of Oklahoma, Norman, OK, USA
c
Laboratories of Molecular Anthropology and Microbiome Research, University of Oklahoma, Norman, OK, USA
ARTICLE INFO
Keywords:
Zooarchaeology
Stable isotopes
Ancient DNA
Anadromous sh
Historical ecology
ABSTRACT
Understanding the habitats people were shing in the past is central to evaluating the relationship between
coastal environmental change and human behavior. Researchers often use zooarchaeological identication of
shes and modern ecological data to infer the habitats people shed in the past. However, these inferences
assume stable environmental conditions through time and can be hindered by precision issues in identication of
archaeological specimens (species vs. genus or family). Here, we integrate genetic and bulk tissue stable isotope
data to investigate a late Holocene sturgeon shery in northern Oregon. Ancient DNA analysis indicated that
people were shing for both green and white sturgeon (Acipenser medirostris and Acipenser transmontanus) in
comparable numbers. Stable isotope analyses of these same bones documented distinct isotope values for each
species, correlating with species-specic habitat preferences. These ndings highlight the value of paired isotope
and genetic data to elucidate human shing strategies and environmental change and provide baseline ecological
data for modern sheries.
1. Introduction
Coastal regions around the world contain a variety of aquatic eco-
systems, ranging from rivers, lakes, and streams to marshes, estuaries,
and fully marine environments, providing a range of animal and plant
species for human subsistence. Evaluating the habitats that people
shed in the past is central for documenting a range of past and present
cultural and environmental issues [see (Casteel, 1976; Wheeler et al.,
1989; Colley, 1990; Morales-Mu˜
niz and Llorente-Rodriguez, 2020)].
These include questions about the types of technologies people were
using through time, evidence for intensication or diversication of
subsistence strategies, and possible anthropogenic or climatic induced
changes to coastal ecosystems. The most common approach for paleo-
environmental reconstruction and inferring past habitats from
zooarchaeological and paleontological assemblages is by extrapolation
from the known ecological preferences of modern sh species (Casteel,
1976; Wheeler et al., 1989). While this comparative approach is essen-
tial for historical ecology investigations, it hinders ne-grained analyses
of generalist shes which may occupy different habitats, or when
taxonomic identications are to genus or family level for functionally
diverse groups (e.g., Sebastes spp. Acipenser spp.).
In this paper, we present stable isotope data from late Holocene
green (Acipenser medirostris) and white (Acipenser transmontanus) stur-
geon from the northern Oregon Coast. Zooarchaeological identication
of eastern Pacic sturgeon is typically done to genus level due to
interspecic similarities between the two species, especially in frag-
mentary specimens [see (Gobalet, 1994; Broughton et al., 2015; Grindle
et al., 2021)]. Prior ancient DNA analysis of the same sturgeon bones we
analyzed here for stable isotopes provided elements identied to species,
with roughly 60% from white sturgeon and 40% from green sturgeon
(Grindle et al., 2021). We explore if bulk tissue stable isotope values vary
between these species, which are known to have overlapping but distinct
habitat preferences (Hildebrand et al., 2016; Moser et al., 2016). Our
work builds on past stable isotope studies of sh specimens from
zooarchaeological collections [e.g. (Szpak et al., 2009; Fuller et al.,
2012; Reitsema et al., 2013; Guiry et al. 2016, 2021; Zangrando et al.,
2016; Braje et al., 2017; Jovanovi´
c et al., 2019; Dombrosky et al., 2020)]
in providing important pre-industrial ecological data of endemic sh, as
* Corresponding author.
E-mail address: ElliottSmithE@si.edu (E.A. Elliott Smith).
Contents lists available at ScienceDirect
Quaternary Science Advances
journal homepage: www.sciencedirect.com/journal/quaternary-science-advances
https://doi.org/10.1016/j.qsa.2022.100062
Received 15 July 2022; Received in revised form 15 September 2022; Accepted 17 September 2022
Quaternary Science Advances 7 (2022) 100062
2
well as inferences into the types of habitats that were used by people
during the late Holocene.
2. Materials and methods
Archaeological context and methods. All archaeological samples used
in this study come from the Par Tee site (35CLT20), located at Seaside,
Oregon about 24 km south of the Columbia River mouth (Fig. 1). The
site was extensively excavated in the late 1960s70s, including 256 1.5
×1.5 m units with roughly 550 m
3
of excavated deposits [see (Sanchez
et al., 2018)]. The deposits appear to have primarily been screened over
¼-inch mesh, with the extensive nature of the excavation producing a
massive assemblage of archaeological faunal remains. These materials
have been the focus of several recent studies, including work on human
subsistence and historical ecology of sea otters, cetaceans, pinnipeds,
shellsh, and nsh (Losey and Power, 2005; Losey and Yang, 2007;
Colten, 2015; Wellman et al. 2017, 2020; Wellman, 2018; Loiselle,
2020; Grindle et al., 2021; Sanchez et al., 2022). These analyses have
been enhanced by high resolution radiocarbon dating of the Par Tee
deposits, which places most of the material at the site between cal AD
100800 (Sanchez et al., 2018).
Subsequent analysis of sh bones from 1/8-inch residuals in bulk soil
samples demonstrated that a range of shes were captured by people
living at the Par Tee site, including sharks, skates and rays (Elasmo-
branchii), rocksh (Sebastes sp.), lingcod (Ophiodon elongatus), cabezon
(Scorpaenichthys marmoratus), atshes (Pleuronectiformes), Pacic
hake (Merluccius productus), salmonids (Oncorhynchus sp.), and sturgeon
(Acipenser spp.) (Sanchez et al., 2022). Grindle et al. (2021) com-
plemented this analysis by studying 1770 sturgeon bones from 98
excavation units distributed across the site. To determine if both green
and white sturgeon were present, ancient DNA analysis was performed
on 30 specimens to determine which species the bones represented.
Specimens were chosen from across the site to minimize the likelihood
of sampling the same individual. Twenty-seven of these samples yielded
DNA, with 16 from white sturgeon (59%) and 11 from green sturgeon
(41%). These 27 samples then formed the basis for the bulk stable
isotope analyses presented here.
Isotopic analysis. We measured δ
13
C and δ
15
N values of bulk bone
protein for the 27 Acipenser specimens previously analyzed for ancient
DNA and identied to species by Grindle et al. (2021). Sturgeon bone
samples were demineralized with 0.25 M hydrochloric acid at 5 C for
48120 h depending on sample size and density; acid was replaced as
needed every 24 h. Samples were then rinsed in deionized H
2
O, lyoph-
ilized, and lipid-extracted via three sequential 24 h soaks in 2:1 chol-
oroform:methanol at room temperature. Lipid extracted samples were
rinsed in deionized H
2
O, lyophilized, and weighed to evaluate percent
protein yield. Following this, 0.50.6 mg of each sample was sealed in a
tin capsule for bulk tissue isotopic analysis.
Bulk bone protein δ
13
C and δ
15
N values, along with weight percent
[C] and [N], were measured via EA-IRMS using a Costech 4010
elemental analyzer (Valencia, CA) coupled to a Thermo Scientic Delta
V Plus isotope ratio mass spectrometer (Bremen, Germany) at the Uni-
versity of New Mexico Center for Stable Isotopes (UNM-CSI; Albu-
querque, NM). All samples and reference materials were calibrated
against the internationally accepted standards for stable carbon and
nitrogen isotope ratios, respectively Vienna-Pee Dee Belemnite (V-PDB)
and atmospheric N
2
(Sharp, 2017). We report all isotopic data as δ
values in parts per thousand, or per mil (), where δ
13
C or δ
15
N =1000*
[(R
samp
/R
std
) 1]. Here, R
samp
and R
std
are the
13
C:
12
C or
15
N:
14
N ratios
of the sample and standard, respectively. The standard deviations of
organic in-house reference materials (milk casein and tuna muscle) were
0.2for both δ
13
C and δ
15
N values. As a control for the quality of our
collagen samples (Ambrose, 1990; Szpak, 2011), we converted
measured weight % [C]:[N] to atomic ratios via the following equation:
[C]:[N]
atomic
=[C]:[N]
weight
×(14/12).
Statistical analysis. We conducted analyses in Program R [v. 4.1.2; (R
Development Core Team, 2021)] with R Studio interface (v. 2022.02.3
+492). We tested assumptions of normality (Shapiro-Wilk) and ho-
mogeneity of variance (F-test) and used unpaired Students t-test to
evaluate differences among A. medirostris and A. transmontanus in δ
13
C
and δ
15
N values. We characterized the isotopic niche space occupied by
each species, as well as the isotopic overlap using Bayesian standard
ellipse areas (Jackson et al., 2011). We calculated the median Bayesian
95% ellipse areas for each group with 95% credibility intervals from 10,
Fig. 1. Location of study area. Adapted from Grindle et al. (2021).
E.A. Elliott Smith et al.
Quaternary Science Advances 7 (2022) 100062
3
000 iterations, discarding the rst 1,000. We express the overlap in
isotopic ellipse area among A. medirostris and A. transmontanus relative
to the sum of non-overlapping ellipse areas as: Overlap in SEA
(SEA1+SEA2)− Overlap. This
metric ranges from a value of 0 (no isotopic overlap) to 1 (complete
isotopic overlap). We computed this metric across 1,000 Bayesian ellipse
area calculations and report the median.
3. Results
We obtained reliable isotopic data for 18 Acipenser specimens
(Table 1). Of the 27 samples we measured, 18 exhibited [C]:[N]
atomic
3.6, 2 exhibited [C]:[N]
atomic
=3.7, and the remaining seven specimens
had [C]:[N]
atomic
from 3.8 to 4.4. The generally accepted range of [C]:
[N]
atomic
values for unaltered bone collagen is between 2.8 and 3.6
(Ambrose, 1990; Szpak, 2011; Guiry and Szpak, 2021). We excluded
specimens with [C]:[N]
atomic
3.7 from subsequent analyses, though we
present all data in Table 1.
Par Tee green sturgeon (A. medirostris) exhibited higher mean δ
13
C
(t
16
=3.5, p <0.01), and δ
15
N values (t
16
=3.0, p <0.01) than white
sturgeon (A. transmontanus) (Fig. 2). The Bayesian standard ellipse areas
of each species, a metric for the ‘isotopic nichealso varied, with white
sturgeon occupying a larger isotopic niche (median SEA
B
[95% CI ] =
3.9
2
[2.2
2
, 7.9
2
]) than green sturgeon (SEA
B
=1.6
2
[0.9
2
,
3.5
2
]). The median proportion of ellipse overlap relative to non-
overlapping areas (0 =no overlap, 1 =complete overlap) was 0.24.
4. Discussion and conclusions
Bulk tissue isotopic measurements and previous genetic research of
archaeological sturgeon bones provide important baseline ecological
data for these endemic sh, as well as the types of species and habitats
that people were targeting in the late Holocene. Green sturgeon are
broadly considered the most marine of all Acipenser, spending most of
their adult lives in estuaries and coastal habitats, and only returning to
freshwater every few years to spawn (Moser et al., 2016). In contrast, the
extent of marine habitat use by white sturgeon is not known (Hildebrand
et al., 2016). Aggregations of white sturgeon do occur in estuarine en-
vironments (Patton et al., 2020), but the species can complete its entire
life cycle within a single river basin (Hildebrand et al., 2016). Adult
green sturgeon are opportunistic consumers of benthic intertidal fauna
(e.g., Neotrypaea californiensis), as well as subtidal crustaceans, bivalves,
and sh (Dumbauld et al., 2008). White sturgeon diets are similarly
broad and vary with size (Muir et al., 1988), including sh such as
lamprey (Lampetra tridentata), eulachon (Thaleichthys pacicus), and
benthic invertebrates (Muir et al., 1988; Dumbauld et al., 2008).
Table 1
Specimen ID Provenience
Taxa* Element % Yield
δ
13
C δ
15
N %N
weight
%C
weight
[C]:[N]
atomic
ACME-91 SW20B7 Acipenser medirostris Cranial 13 12.6 18.5 16 44 3.2
ACME-101 SW20G6 Acipenser medirostris Cranial bone 14 12.3 16.5 16 45 3.3
ACME-110 NE8B6 Acipenser medirostris Cranial 11 13.0 17.2 16 45 3.4
ACME-95 SE6D7 Acipenser medirostris Scute fragment 8 13.0 16.7 16 46 3.4
ACME-107 NE10D4 Acipenser medirostris Cranial 12 12.8 15.7 15 46 3.5
ACME-93 SE8I10 Acipenser medirostris Pectoral girdle 9 13.2 17.1 12 37 3.5
ACME-89 SW20A8 Acipenser medirostris Scute fragment 10 13.5 17.9 15 46 3.5
ACME-90 SW20B6 Acipenser medirostris Scute fragment 16 14.1 16.6 9 29 3.6
ACME-100 SE6D5 Acipenser medirostris Fragment 7 14.1 16.2 13 43 3.7
ACME-88 NE17G7 Acipenser medirostris Cranial 8 15.2 17.6 13 44 4.0
ACME-92 NE8B5 Acipenser medirostris Cranial 7 15.9 16.8 14 46 4.0
ACME-99 SW20G2 Acipenser medirostris Fragment; not scute 15 17.9 14.6 11 42 4.4
ACTR-85 NE7I8 Acipenser transmontanus Scute fragment 11 16.0 14.2 16 45 3.3
ACTR-102 SE13L6 Acipenser transmontanus Scute 14 13.8 17.0 16 45 3.3
ACTR-103 SE13L7 Acipenser transmontanus Pectoral girdle 12 14.9 15.5 16 45 3.3
ACTR-113 SW20A6 Acipenser transmontanus Scute 13 15.6 13.6 16 46 3.3
ACTR-105 NE17F5 Acipenser transmontanus Scute 15 13.8 15.5 17 50 3.4
ACTR-86 NE7I6 Acipenser transmontanus fragment 10 13.2 14.3 15 45 3.4
ACTR-87 NE8H6 Acipenser transmontanus Scute 13 15.1 15.7 16 45 3.4
ACTR-97 SE5K10 Acipenser transmontanus Scute fragment 8 15.5 14.6 15 44 3.4
ACTR-98 NE7C7 Acipenser transmontanus Fragment 9 12.8 17.6 14 44 3.5
ACTR-109 SE8I5 Acipenser transmontanus Cranial 9 15.0 16.4 14 45 3.6
ACTR-108 SE8I7 Acipenser transmontanus Fragment 9 15.4 15.8 14 43 3.7
ACTR-106 NE10D3 Acipenser transmontanus Scute 13 16.4 14.8 13 43 3.8
ACTR-111 NE10D6 Acipenser transmontanus Scute fragment 7 14.1 16.5 13 44 3.8
ACTR-104 SE13L9 Acipenser transmontanus Scute 7 16.0 14.8 14 46 3.8
ACTR-96 SE5K8 Acipenser transmontanus Scute 9 15.3 16.2 13 43 3.8
Unit and level specimen was recovered from, as in Grindle et al. (2021).
* Taxonomic identications from Grindle et al. (2021).
Calculated as: [(mass of specimen post demineralization, lipid extraction, and lyophilization) ÷initial mass of specimen] ×100.
Specimens with [C]:[N]
atomic
values 3.7 have likely undergone signicant diagenetic alteration (Ambrose, 1990; Szpak, 2011) and were not included in statistical
analyses or data interpretation.
Fig. 2. Isotopic niche space of archaeological sturgeon specimens. Shown are
bulk tissue carbon (δ
13
C) and nitrogen (δ
15
N) values of green (A. medirostris;
green circles) and white (A. transmontanus; white circles) sturgeon. Ellipses
represent 50% of the total amount of bivariate isotope space occupied by each
species. (For interpretation of the references to colour in this gure legend, the
reader is referred to the Web version of this article.)
E.A. Elliott Smith et al.
Quaternary Science Advances 7 (2022) 100062
4
Our analyses of sturgeon from Par Tee support this existing body of
knowledge while providing new insights through stable isotope analysis
from a pre-industrial context. Green sturgeon recovered from the site
had high δ
13
C and δ
15
N values (Fig. 2) and occupied a small isotopic
niche space (1.6
2
), indicating minimal ecological variation among
individuals. Generally, species living or foraging in marine/estuarine
ecosystems tend to have higher δ
13
C and δ
15
N values than those in
freshwater habitats (Hobson, 1999), a pattern observed in populations
of both modern Acipenser (Gu et al., 2001; Sulak et al., 2012) and their
prey (Stewart et al., 2004; Zeug et al., 2014). Our results thus suggest
that green sturgeon in the past were heavily reliant on marine envi-
ronments and had similar ecological preferences to what is observed
today.
In contrast, white sturgeon from Par Tee exhibited a much larger
isotopic niche (3.9
2
) and lower mean δ
13
C and δ
15
N values (Fig. 2),
suggesting a freshwater preference for the species (Hobson, 1999). A
closer examination reveals two distinct clusters of white sturgeon in
bivariate δ
13
C and δ
15
N space one group with lower δ
13
C and δ
15
N
values, and one group with higher values. The former matches δ
15
N
values of modern white sturgeon collected in San Francisco Bay (Stewart
et al., 2004; Zeug et al., 2014). The δ
13
C values of Par Tee sturgeon are
higher than observed in modern individuals, though this may result from
a combination of temporal [~1.52.0 (Dombrosky, 2020)], and
tissue-specic [~1.05.5 (Sholto-Douglas et al., 1991; Guiry and
Hunt, 2020);] isotopic differences.
The second grouping of Par Tee white sturgeon maps onto our
measured isotopic niche for green sturgeon (Fig. 2). One possible
explanation for this is consumption of migrating salmonids or eulachon,
which is supported by movement patterns of modern white sturgeon
(Hildebrand et al., 2016), and could serve to increase δ
13
C and δ
15
N
values. However, seasonal consumption of anadromous sh is unlikely
to be the sole explanation as the turnover rate of bone is slow, and
collagen isotope values reect decades of dietary information in a long
lived species (Hobson and Clark, 1992; Hedges et al., 2007). Instead, our
data suggest potential habitat segregation among white sturgeon in the
past, with some individuals foraging predominantly in freshwater, and
others in coastal or marine environments. However, substantial isotopic
variability exists within both freshwater and marine ecosystems (Fuller
et al., 2012; Sulak et al., 2012; Guiry, 2019), and studies employing
essential amino acid δ
13
C analyses [e.g. (Larsen et al., 2009, Elliott
Smith et al., 2022)] are needed to conrm marine resource use by
archaeological A. transmontanus. These studies could be paired with
population genetic studies of both ancient and modern sturgeon to
explore potential correlations among population structures and isotopic
(e.g., dietary) niches (Cook et al., 2007; Brophy et al., 2020).
Previous studies of Par Tee (Colten, 2015; Grindle et al., 2021;
Wellman, 2021; Sanchez et al., 2022) have highlighted the diversity of
species and environments used by local people. Our isotopic measure-
ments of Par Tee sturgeon demonstrate that these sh were ultimately
sourced from a combination of marine and freshwater/estuarine envi-
ronments and by extension people were utilizing resources from these
habitats. However, it is unclear precisely where people obtained sur-
geon. A large range of aquatic habitats existed historically in the Seaside
region (Fig. 1) including coastal reefs, freshwater streams such as the
Neawanna Creek and Necanicum River, a small embayment to the open
ocean, and the massive Columbia River estuary about 24 km north (see
Colten, 2015; Sanchez et al., 2022). Sturgeon could potentially have
been taken from all these habitats using a variety of shing methods (e.
g., seines and nets, harpoons, and hook and line; Grindle et al., 2021;
Sanchez et al., 2022). Indeed, the lower Columbia River (south of
Bonneville Dam) is a known spawning and foraging area for modern
populations of white sturgeon (McCabe Jr and Tracy, 1994; Parsley
et al., 2008). Given the wide range of marine, freshwater, and terrestrial
fauna available in the Par Tee assemblage (Colten, 2015; Sanchez et al.,
2022), we suspect people were strategically and opportunistically
obtaining sturgeon during sh migrations or summer foraging
aggregations (see Parsley et al., 2008).
More broadly, our study highlights the importance of pairing genetic
and isotopic analyses when studying faunal remains from archaeological
or subfossil contexts; isotopic data alone would have incorrectly inferred
several white sturgeon samples to be green sturgeon (Fig. 2), and genetic
analyses cannot provide evidence of long-term consumer habitat use and
diet. Pre-industrial data on sturgeon ecology (Fuller et al., 2012; Reit-
sema et al., 2013; Jovanovi´
c et al., 2019) are valuable for the manage-
ment of modern sheries, as ecological studies of Acipenser have been
predominantly conducted in highly altered habitats (Gu et al., 2001;
Secor et al., 2002; Sulak et al., 2012; Zeug et al., 2014; Hildebrand et al.,
2016; Bruestle et al., 2019). Interdisciplinary analyses have great po-
tential for future studies of the past hunting and shing strategies of
people and the historical ecology of native fauna.
Declaration of competing interest
The authors declare that they have no known competing nancial
interests or personal relationships that could have appeared to inuence
the work reported in this paper.
Data availability
All data are available in the text (Table 1).
Acknowledgements
We are grateful to Laura Burkemper and Viorel Atudorei at UNM CSI
for assistance with bulk isotope analyses, and Amanda Lawrence at
NMNH MSC for help with collections. We also thank Jon Dombrosky for
many helpful discussions and his icthyoarchaeology enthusiasm. We
thank Nihan Dagtas, Hannnah Wellman and Rita Austin for their con-
tributions to the ancient DNA analysis. We thank Ken Gobalet, Dalyn
Grindle, Rob Losey, and Gabe Sanchez for providing insights about the
Par Tee sh assemblage. EES was supported by a National Science
Foundation Postdoctoral Research Fellowship in Biology (DBI-1907163)
and a Smithsonian NMNH Peter Buck Postdoctoral Fellowship.
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